Plant Cell Rep DOI 10.1007/s00299-016-1949-3

REVIEW

Cytoplasmic male sterility (CMS) in hybrid breeding in field crops Abhishek Bohra1 • Uday C. Jha1 • Premkumar Adhimoolam1 • Deepak Bisht2 Narendra P. Singh1

•

Received: 30 November 2015 / Accepted: 2 February 2016 Ó Springer-Verlag Berlin Heidelberg 2016

Abstract Key message A comprehensive understanding of CMS/ Rf system enabled by modern omics tools and technologies considerably improves our ability to harness hybrid technology for enhancing the productivity of field crops. Abstract Harnessing hybrid vigor or heterosis is a promising approach to tackle the current challenge of sustaining enhanced yield gains of field crops. In the context, cytoplasmic male sterility (CMS) owing to its heritable nature to manifest non-functional male gametophyte remains a cost-effective system to promote efficient hybrid seed production. The phenomenon of CMS stems from a complex interplay between maternally-inherited (mitochondrion) and bi-parental (nucleus) genomic elements. In recent years, attempts aimed to comprehend the sterilityinducing factors (orfs) and corresponding fertility determinants (Rf) in plants have greatly increased our access to candidate genomic segments and the cloned genes. To this end, novel insights obtained by applying state-of-the-art omics platforms have substantially enriched our understanding of cytoplasmic-nuclear communication. Concomitantly, molecular tools including DNA markers have

Communicated by N. Stewart.

Electronic supplementary material The online version of this article (doi:10.1007/s00299-016-1949-3) contains supplementary material, which is available to authorized users. & Abhishek Bohra [email protected] 1

Indian Institute of Pulses Research (IIPR), Kanpur, India

2

National Research Centre on Plant Biotechnology (NRCPB), New Delhi, India

been implicated in crop hybrid breeding in order to greatly expedite the progress. Here, we review the status of diverse sterility-inducing cytoplasms and associated Rf factors reported across different field crops along with exploring opportunities for integrating modern omics tools with CMS-based hybrid breeding. Keywords Cytoplasm  Sterility  Fertility  Hybrid  DNA marker  Genome  Gene

Introduction In plants, the cytoplasmic male sterility (CMS) is ascribed to the maternally inherited inability to establish a genomic harmony between the organellar (mitochondrial) and nuclear genomes (Touzet and Budar 2004; Fujii and Toriyama 2008; Touzet and Meyer 2014). This impaired cytoplasmic-nuclear communication results in the production of non-functional pollen grains (Hanson and Bentolila 2004). The CMS is reported in over 150 plant species (Laser and Lersten 1972) existing either as a spontaneous machinery (Hanson and Bentolila 2004) or it can be created through experimental means like induced mutations, wide/ inter-specific hybridization, protoplasmic fusion and genetic engineering (Yamagishi and Bhat 2014; Wang et al. 2013a; Singh et al. 2015). With respect to field crops, cytoplasmic sterility prevails across several species encompassing major dietary staples like rice, maize as well as lesser-researched crops such as pigeonpea and faba bean. Parallel with the discovery of sterile cytoplasms, restorer-of-fertility (Rf) genes have been identified in various crops as the genetic means that enable reconciliation of the lost genomic harmony between the two genomes. To this end, a subset of these cytoplasm-specific

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Rf genes has already been cloned in different field crops using map-based cloning approach (Dahan and Mireau 2013). In view of the shared evolutionary dynamics, the CMS-Rf system mimics Flor’s ‘‘gene-for-gene’’ model that explains in sync progression of host plant resistance and pathogen avirulence (Touzet and Budar 2004; Dahan and Mireau 2013; Chen and Liu 2014; Tan et al. 2015). CMS circumvents the need for removal of anthers, thereby encouraging hybrid technology to generate dramatically superior F1 progenies that exhibit significant advantage over its parents and existing popular cultivars in terms of yield, stress tolerance, adaptability etc. (Saxena et al. 2013; Reddy et al. 2006). In rice, presence of two restorer loci in hybrid was found to be associated with higher tolerance to low temperature (Huang et al. 2012). In general, greater yield stability of hybrids over line varieties was established in both self- (Longin et al. 2012; Mu¨hleisen et al. 2014) and cross-pollinating crops (Le´on 1994). However, contrasting results with hybrids showing lower yield stability were also reported (Mu¨hleisen et al. 2015; see Mette et al. 2016 and references therein). While advocating the view of greater yield stability of hybrids, Mu¨hleisen et al. (2014) suggested undertaking more comprehensive studies that derive concrete inferences from the data recorded over several years on multiple locations. Further, incorporating novel traits of dominant nature into parental lines may be a convenient means for eventually combining the multiple resistant phenotypes in the derived F1s (Reddy et al. 2006; Cheng et al. 2007). Given the substantial contribution of crop hybrids to current food production systems, CMS-based hybrid technology remains a promising approach to sustain enhanced crop productivity (Wang et al. 2013a; Whitford et al. 2013; Horn et al. 2014). In this review, we begin with a retrospective view on the discovery of diverse sterilizing cytoplasms in selected field crops. Accompanying this, genetic determinants responsible for the CMS and fertility restoration are briefly discussed. An emphasis is placed on capturing critical findings obtained recently by means of next generation sequencing (NGS) assisted omics technologies. Finally, we highlight scope for accelerating CMS hybrid breeding using modern omics tools.

the fact that both lines (A and B) differ only for sterilityinducing cytoplasm. In other words, A 9 B scheme in CMS programme regenerates the genetic constitution of A-line (Whitford et al. 2013) and hence, as an essential prerequisite B-line must be devoid of any Rf gene. Whereas, F1 products of A 9 R cross are able to resume fertility and often exhibit substantially improved performance i.e. hybrid vigour. The CMS has emerged as a boon to harness the hybrid technology in crop plants owing to its distinctive ability that creates sterile male gametophyte in plant without exerting any depression on its agronomic performance (Feng and Jan 2008; Fujii and Toriyama 2008; Lin et al. 2014; Touzet and Meyer 2014) as evident from a comparison of performance between A 9 R and B 9 R crosses (Ramesh et al. 2006); though instances have been reported where the sterile cytoplasm also exhibited pleiotropic effects on female fertility (Manickam et al. 2010), flower structure, chlorophyll content and yield (Kaul 1988). Table 1 provides a list of hybrids developed in India using CMS/Rf system. Once discovered, the sterilizing cytoplasm can be transferred to any genetic background using a standard backcrossing protocol with the candidate background (nucleus donor) recurrently exploited as the pollen parent (see Chase 2007; Khan et al. 2015; Atri et al. 2016). Searching for potential R-lines, however, warrants extensive fieldtesting of large-scale A 9 R progenies (Serieys 1996; Jordan et al. 2010; Bohra et al. 2012) or R 9 R or transferring fertility-governing factors to diverse backgrounds. More often, a restorer is recovered from the same interspecific population, in which the sterilizing cytoplasm was originally discovered or can be gained from wild parent/ other wild relatives (Serieys 1996; Feng and Jan 2008). Moreover, the potential use of R line is sometimes impeded by the undesirable linkage drag mending of which requires considerable time and efforts (Primard-Brisset et al. 2005). To this end, advances in DNA marker technologies have helped tremendously in the expeditious recovery of A-, Band R-lines along with facilitating fast-track introgression of the genomic segment tightly associated with male sterility or fertility. Discovery of sterilizing cytoplasms in field crops: a retrospect

Three-line (A, B, R) breeding for harnessing hybrid vigor Operationally, the CMS system relies on three components (Chen and Liu 2014). The genotypes carrying sterilizing (mitochondrion-derived) and Rf (nucleus-encoded) factors are referred to as sterile (A) and restorer (R) lines, respectively. The third line ‘maintainer’ (B) is essentially required to retain the male sterile status of A-line owing to

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As indicated by Havey (2004), southern corn leaf blight (an outbreak reported in the case of maize CMS-T) constitutes an exemplary demonstration to underscore crop’s genetic vulnerability growing proportionately with the widespread cultivation of hybrids based on single cytoplasmic source. Given the context, a range of stable sterile cytoplasms was reported in different field crops in order to avoid the possible occurrence of such disease epidemics. Here we

Plant Cell Rep Table 1 A non-exhaustive list of CMS-based hybrids developed in different field crops in India Crops

Predominant Cytoplasm

Hybrids*

References/links

Rice

WA-CMS

Pusa RH 10 (2001), Narendra Usar Sankar Dhan 3 (2004), Ajay (CRHR 7) (2005), DRRH 2 (2005), Sahyadri 2 (2005), Sahyadri 3 (2005), CORH-3 (2006), HKRH-1 (2006), JRH-4 (2007), JRH-5 (2007), Sahyadri – 4 (2008), DRRH- 3 (2009), CO– RH-4 (2011), PNPH 24 (2012); CR Dhan 701 (2012)

www.icar.org/www.iari.res.in; www.crri.nic.in; www. drricar.org; Das et al. (2014); Ingale et al. (2006); www.jnkvv.nic.in; www.icar.org; www.tnau.nic.in; http://www.rkmp.co.in/content/hybrid-rice?page= show;

Sunflower

Kalinga I CMS PET1-CMS

Rajalaxmi (2005) TCSH-1 (2000), KBSH-41 (2001), NDSH-1 (2003), LSFH-35 (2003)

www.crri.nic.in www.tnau.ac.in/cpbg/oilseeds/sunflower-varieties; Dudhe et al. (2011); http://oilseeds.dacnet.nic.in/ Sunvar.html

A1 or milo (Reddy et al. 2012)

CSH 1 (1964), CSH19R (2000), CSH 25 (2008), CSH27 (2011), SPH-1629 (2012), CSH28 (2012)

www.icar.org.in; Singh and Lohithaswa (2006); Hariprasanna and Patil (2015)

Sorghum

Brassica

Moricandia

NRCHB 506 (2008)

www.drmr.org.in

Pearl millet

A1-CMS

HHB 67-2 (improved version of HHB 67) (2005); MH 1234 (2006); Nandi-52 (2008); Shine (MH-1578) (2012); Kaveri super boss (MH 1553)(2013); MPMH 17 (MH 1663) (2014); Pratap (MH 1642) (2014);

www.icrisat.org; www.icar.org; www.aicpmip.res.in; www.nandiseed.com; http://smis.dacnet.nic.in/

Pigeonpea

A2-CMS (Cajanus scarabaeoides)

GTH1 (2004)

Saxena et al. (2011, 2013)

ICPH 2671 (Pushkal) (2010)

A4-CMS (Cajanus cajanifolius) *

Year of release is given in parenthesis

discuss some of the important sterile cytoplasm discovered in the selected crops. Rice Following Weeraratne (1954) reporting the first instance of sterile cytoplasm in rice, CMS-BT (Boro type) was identified from an indica variety ‘Chinsurah Boro II’ (Shinjyo and Omura 1966). However, the true potential of CMS was realized after the discovery of CMS-WA (Wild Abortive) in spontaneous wild population of Oryza sativa spontanea (see Lin and Yuan 1980). The use of WA cytoplasm has been preferred for hybrid breeding in rice given the advantage of sporophytic system. Alternate CMS systems to CMS-WA were also established in rice (Huang et al. 2014) some of which are listed in Table 2.

susceptibility of to Southern corn leaf blight, which became evident during 1970. Although additional sterilizing cytoplasms like CMS-S (CMS-USDA) and CMS-C (CMSCharrua) were reported in maize (Table 2), breeders nowadays prefer single cross hybrids instead of the CMSbased hybrids (http://agridaksh.iasri.res.in/). Wheat Sterile cytoplasm appeared in wheat as an outcome of a hybridization event involving Triticum aestivum and T. timopheevi. To date, more than 70 kinds of CMSs have been reported in wheat (Liu et al. 2006). A search for a ‘‘definitive’’ CMS system has recently led to the development of msH1 in wheat using Hordeum chilense as the cytoplasm donor (Martin et al. 2008).

Maize

Brassica

With the discovery of CMS-T (CMS-Texas) in OPV Golden June (Rogers and Edwardson 1952), CMS emerged as a viable procedural option to manual detasseling. However, CMS-T was completely removed from maize hybrid breeding schemes due to its widespread

Subsequent to the discovery of the Ogura CMS in Japanese radish (Ogura 1968), the sterile cytoplasm was transferred to different cultivars of Brassica and radish using backcross scheme. The Ogura cytoplasm is widely used in hybrid breeding of Brassica napus and B. juncea (Yamagishi and

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Soybean

Sorghum

Sunflower

RN, ZD, N8855

G. max

Milo (Durra race) IS1112C

A1 (milo)

H. tuberosus H. petiolaris sp fallax

CMS 514A

CMS PEF1

A3

H. giganteus

CMS GIG2

Yunnan purple rice

ZidaoA (CMS-ZD) Helianthus petiolaris H. giganteus

O. rufipogon

RT98 A

CMS-PET1 CMS GIG1 (CMG2)

O. perennis O. rufipogon

K52

K-type

IR66707A

Dianyu 1 A

CMS-D

RT102A

O. rufipogon

FA-CMS

Gambiaca (indica) 9 Chaoyang 1 (indica)

Gambiaca

O. rufipogon

CW-CMS

O. sativa

O. rufipogon

HL-CMS

CMS-GA

Oryza sativa sp. spontaneae

WA-CMS

Kalinga-I, Lalruma

Chinese wild rice 9 Fujisaka 5 (japonica variety)

Lead Rice (Burmese indica variety)

LD-CMS

G. max 9 G soja, N8855 9 N2899

–

Milo (land race) 9 Kafir (land race)

H. petiolaris sp fallax 9 H. annuus

H. tuberosus 9 Inbred line 7718B

H. giganteus (accession1934) 9 H. annuus (cv. HA 89)

Helianthus petiolaris 9 Amavirskii 3491 H. giganteus 9 H. annuus

–

O. rufipogon (W1109) 9 O. sativa (Taichung 65)

O. rufipogon (W1125) 9 O. sativa (Taichung 65)

O. perennis 9 IR64

K52 (japonica) 9 Fenglongzao/Qing’er’ai (indica)

Dissi (indica) 9 Zhenshan 97 (indica)

Dongxiang wild rice 9 Zhongzao 35 (indica variety)

Kalinga-I 9 Krishna, Lalruma 9Krishna

O. rufipogon 9 Lian Tang Zao (indica variety)

O. sativa sp. spontaneae 9 Hsien (indica) O. sativa sp. spontaneae 9 Keng (japonica)

Lead rice (Burmese indica variety) 9 Fujisaka 5 (japonica variety)

Chinsurah Boro II (indica) 9 Taichung 65 (japonica)

Chinsurah Boro II (indica variety)

BT-CMS

Cross

Rice

Donor

Cytoplasm

Crop

Table 2 List of diverse male sterility inducing cytoplasms/lines established in different field crops along with the cytoplasm donors

see Dong et al. (2012) and references therein

Tang et al. (2007)

Stephens and Hollard (1954)

Serieys and Vincourt (1987)

Liu et al. (2013a)

Feng and Jan (2008)

Leclercq (1969) Whelan (1981)

Hu et al. (2013)

Igarashi et al. (2013)

Okazaki et al. (2013)

Dalmacio et al. (1995)

Huang et al. (2014)

Tao et al. (2004)

Xian-hua et al. (2013)

Pradhan et al. (1990); http:// www.iisc.ernet.in/currsci/ may10/articles21.htm

Huang et al. (2014)

Katsuo and Mizushima (1958)

see Huang et al. (2014) and reference therein

Lin and Yuan (1980)

Watanabe et al. (1968)

Shinjyo and Omura (1966)

References

Plant Cell Rep

Brassica

Wheat

Spontaneous CMS variants in Xiangyu (B. napus) Bronowski or Hokuriku 23(B. napus)

681A

Nap CMS

–

–

–

S. arvensis 9 B. napus

Sinapis arvensis Spontaneous male sterile mutant in B. juncea

Nsa CMS

Hau CMS Line (00-6102A)

–

Polima spring variety of B. napus

– Mori-cytoplasm into Brassica juncea –

Polima CMS

CA8057

YA-type

T. timopheevi 9 T. aestivum –

Moricandia arvensis Japanese radish

Ae. kotschyii

Mori-cytoplasm Ogura CMS

Triticum timopheevi

K-type

MB177 (G. hirsutum) 9 {(G. hirsutum 9 G. thurberi) 9 (G. arboreum 9 G. hirsutum)}

G. thurberi G. arboreum

T-cytoplasm

–

G. hirsutum

JA-CMS

G. harknessii 9 G. hirsutum, AD1 G. trilobum 9 Gossypium hirsutum

Gossypium harknesii G. trilobum

CMS-D2

–

–

–

Cross

CMS-D8

Teopod maize Charrua (Brazilian maize)

CMS-S (USDA Cytoplasm)

CMS-C (Charrua cytoplasm)

Cotton

Golden June (Mexican OPV)

CMS-T (Texas Cytoplasm)

Maize

Donor

Cytoplasm

Crop

Table 2 continued

Budar et al. (2006)

Liu et al. (2005)

Wan et al. (2008); Heng et al. (2014)

Yan et al. (2013)

Li et al. (2011)

Chanderasekhara et al. (2013) Ogura (1968); see Yamagishi and Bhat 2014

Liu et al. (2006)

Liu et al. (2011)

Wilson and Ross (1962)

Yang et al. (2014)

Stewart (1992)

Meyer (1975)

Beckett (1971)

Jenkins (1978)

Rogers and Edwardson (1952)

References

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123 C. cajanifolius C. cajan

C. lineatus C. platycarpus C. reticulatus

A4

A5

A6

A7

A8

– English bean population FAB 199 (Accession from Afghanistan) FAB 297 (Accession from Egypt)

CMS 447

CMS 199

CMS 297

Faba bean

G08063

CMS 350

CMS-Sprite

Male sterile plant of Large Seeded Gene Pool (LSGP)

A5 CMS system

Common bean

– Senegalese accession of Pennisetum glaucum (L.) R. Br. subsp. monodii

A2 and A3 cytoplasm

A4 CMS

Tift 23A

C. volubilis

A3

A1

C. scarabaeoides

A2

Pearl millet

Cajanus sericeus

A1

Pigeonpea

Donor

Cytoplasm

Crop

Table 2 continued

FAB 297 9 FAB 70

FAB 199 9 FAB 187

–

–

CMS-G08063 9 Sprite

–

–

–

–

C. reticulatus (ICPW 176) 9 C. cajan (ICP 28, ICPL 87119 and ICPL 20176)

C. platycarpus (ICPW 68) 9 ICPL 85010

C. lineatus 9 ICPL 99044

C. cajan 9 C. acutifolius (ICPW 15613)

ICPW 29 9 ICPL 28

C. volubilis 9 a cultivated type

C. scarabaeoides 9 ICPL 85030

C. sericeus 9 advanced breeding line of pigeonpea

Cross

Link et al. (1997)

Berthelem and Guen (1974) See Link et al. (2008)

Bond et al. (1966)

Bassett and Shuh (1982); Mackenzie et al. (1988)

Rai (1995)

Hanna (1989)

Rai et al. (2001)

Burton (1958); Singh (1995)

Saxena (2013)

Mallikarjuna et al. (2006)

Saxena et al. (2010a)

Mallikarjuna and Saxena (2002, 2005); Rathnaswamy et al. (1999)

Rathnaswamy et al. (1999); Saxena et al. (2005)

Wanjari et al. (1999)

Ariyanayagam et al. (1993); Tikka et al. (1997); Saxena and Kumar (2003); Kalaimagal et al. (2008)

Ariyanayagam et al. (1993)

References

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Bhat 2014; Bisht et al. 2015). Further, polima (pol) CMS of B. napus offers another well-known example of spontaneous male sterility. In case of B. juncea, sexual and somatic hybridization with wild relatives delivered diverse CMS lines (Prakash et al. 1998). More recently, a new CMS ‘fruti’ was discovered in B. juncea using B. fruticulosa as the cytoplasm donor (Atri et al. 2016).

1958). Subsequently A2- and A3-CMSs were further developed as an attempt to diversify the CMS, however an inferior performance compared to A1 restricted their extensive use in crop improvement (Rai et al. 2001). Additional CMSs in sorghum include A4 (Hanna 1989) and A5 (Rai 1995). Cotton

Sunflower The discovery of CMS-PET1 was reported from the wild species Helianthus petiolaris (Leclercq 1969), Although more than 70 CMS have been reported so far in sunflower (Liu et al. 2012b), only the CMS-PET1 has been exclusively employed for developing hybrids (Reddy et al. 2008). Serieys (1996) has synthesized a comprehensive report on the CMS aspect of sunflower by cataloguing the diverse sterilizing cytoplasms, associated Rf genes and their inheritance patterns. Soybean The initial CMS in soybean was derived through a hybridization event between Glycine max (accession 167) and G. soja (accession 035) (Sun et al. 1994). The alternative sterile cytoplasms discovered in germplasm include Ru Nan Tian Dan, ZD8319, N8855, XXT, N21566, N23168, ZD8319 and XXT (Li et al. 1995; Ding et al. 1998; Zhao et al. 1998; Gai et al. 1995, 1999; Zhang and Dai 1997; Palmer et al. 2010; Bai and Gai 2005; Zhao and Gai 2006; Wang et al. 2010a). However, the commercialscale implementation of CMS for hybrid development often faces impediments like dearth of robust CMS/Rf system, inadequacy of pollen donors and insect vectors (Graybosch and Palmer 1985). Sorghum The milo CMS (designated as A1) placed into kafir nuclear background represents the first CMS in sorghum (Stephens and Holland 1954; Reddy et al. 2012). Subsequently, alternate types of sterilizing cytoplasms were also reported in sorghum viz, A2 (Guinea, Caudatum) (Schertz and Ritchey 1978); A3 (Durra, Caudatum, Kafir-Caudatum) (Quinby 1980), A4 (Guinea) (Worstell and Kidd HJ Schertz 1984); Indian A4 (A4 M, A4 VZM, A4G) (Rao et al. 1984), A5 (bicolor), A6 (durra) (Schertz et al. 1997) and 9E (Webster and Singh 1964; Ross and Heckerott 1972). Pearl millet CMS hybrid breeding in pearl millet came into existence after the discovery of A1-CMS i.e. Tifton 23A (Burton

The Gossypium harknesii cytoplasm was transferred to G. hirsutum background through repeated backcrossing accompanied by selection, and the CMS thus obtained was referred to as D2 (Meyer 1975). Later, D8 was obtained by introducing G. trilobum cytoplasm into G. hirsutum, while G. aridum and G. sturtianum are among additional CMS sources reported in cotton (Stewart 1992). Common bean The CMS-sprite has been intensively researched in common bean. However, despite registering nearly 47 % heterosis for seed yield hybrid breeding could not gain widespread acceptance due to difficulties encountered in large-scale production (Palmer et al. 2011). Pigeonpea Eight sterilizing cytoplasms designated as A1-A8 CMS were thus far reported in pigeonpea (Bohra et al. 2010; Saxena et al. 2010a). Of these, only two i.e. A2 and A4 are being currently used in hybrid development given the stability of male sterility and availability of promising B- and R-lines (Saxena 2013).

The genetic architecture of fertility-restoration trait in plants Genetic inheritance and molecular mapping of Rf genes To decipher the genetic determinants that control fertility restoration trait, inceptive genetic analyses relied predominantly upon Mendelian genetics, and to a large extent, successfully explained the underlying genetic control using simple mono-/di- genic models often accompanied by conventional allelism tests. The restoration phenomenon in WA-CMS is accounted to two separate Rf genes with dominant inheritance (Zhou 1983; Govinda and Virmani 1988; Bharaj et al. 1991; Teng and Shen 1994; Zhang et al. 2002). Analysis of Rf loci in WA-CMS rice reflected its digenic nature with the responsible genetic determinants located on chromosomes 7 and 10 (Bharaj et al. 1995).

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Employment of diverse marker technologies has served to determine genomic location of Rf genes (Supplementary Table). For example, in rice two Rf genes of dominant nature i.e. Rf3 and Rf4 were mapped on chromosome 10 using restriction fragment length polymorphism (RFLP) technology (Zhang et al. 2002). Likewise, RFLP and random amplified polymorphic DNA (RAPD) markers were employed to map Rf3 gene on chromosome 1 (Yao et al. 1997; Zhang et al. 1997). Two additional QTLs (Tan et al. 1998a) and Rf gene (Tan et al. 1998b) were mapped on rice chromosome 10, while Sheeba et al. (2009) assigned Rf4 locus to chromosome 10. In HL-CMS, two restorer loci Rf5 and Rf6 (t) were detected on chromosome 10 (Liu et al. 2004) apart from the single dominant restorer Rf5 gene reported earlier by Huang et al. (2000, 2003). A novel restorer locus Rf 6 was later mapped on the short arm of chromosome 8 (Huang et al. 2012). The BT-CMS preferred mostly for japonica hybrid breeding (Fujimura et al. 1996) is restored gametophytically by a single dominant Rf1 gene (Shinjyo 1975; Iwabuchi et al. 1993; Komori et al. 2003) on chromosome 10 (Kinoshita et al. 1995; Ichikawa et al. 1997). A new Rfcw gene restoring CW-CMS gametophytically was mapped on chromosome 4 (Fujii and Toriyama 2005) and this chromosome also harbored Rf17 gene (Fujii and Toriyama 2009). A trisomic analysis in LD-CMS elucidated that the Rf2 gene on chromosome 2 resumed fertility in a gametophytic fashion (Shinjyo and Sato 1994). As discussed by Huang et al. (2014), most of the Rf genes cloned to date act in a dominant fashion except for Rf17 gene in CW-CMS rice (cloned by Fujii and Toriyama 2009) where ‘‘loss-of-function’’ of the candidate Rf gene (suppressed expression of ORF11) was reported to cause fertility restoration. In maize, two genes Rf1 and Rf2 conditioning fertility to CMS-T (Duvick 1965; Levings 1993) were mapped on chromosomes 3 (Wise et al. 1996) and 9, respectively (Wise and Schnable 1994). Later, the fertility recovery of CMS-T was reported to be influenced by the cumulative action of Rf1 and Rf2a (Wise et al. 1999). The case of partial fertility recovery was also documented in the CMST in the presence of genes Rf8 and Rf* with Rf2a (Dill et al. 1997). Recently, complete or partial fertility of the CMS-T recovered by Rf2a gene in association with Rf1, Rf8 or Rf* genes was also investigated (Meyer et al. 2011). Fertility restoration of S-CMS is caused by dominant gene Rf3 acting in a gametophytic manner (Buchert 1961; GabayLaughnan et al. 1995; Kamps et al. 1996; Zabala et al. 1997), which was later mapped on chromosome 2 (Laughnan and Gaby 1978; Kamps and Chase 1997; Gabay-Laughnan 2004; Zhang et al. 2006). In relation to CMS-C, the restoration was accounted to the sporophyticmode action of a single dominant gene Rf4 (Kheyr-pour

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et al. 1981), which was later placed onto chromosome 8 (Sisco 1991). In addition to family-based mapping, genome wide association study (GWAS) of maize association panel comprising testcross hybrids profiled a total of 30 QTLs with variable phenotypic effects for pollen-related traits. The recovery of several minor effect QTLs excepting Rf 3 led authors to advocate a polygenic model illustrating the genetic composition of fertility trait in CMS-S (Feng et al. 2015). In wheat, the RFLP analysis of Rf3 gene that controlled fertility retrieval in T. timopheevi CMS assigned this gene to the short arm of chromosome 1B (Kojima et al. 1997; Zhou et al. 2005). A major QTL restoring fertility on chromosome 1B and the minor QTLs scattered across 2A, 4B, and 6A chromosomes were detected for fertility restoration (Ahmed et al. 2001). While, two dominant Rf genes impacting upon T. timopheevi-CMS were mapped on short arms of chromosomes 1A and 1B (Zhang et al. 2003). A new restorer gene Rf8 imparting fertility to T. timopheevi-CMS was assigned to the short arm of chromosome 2D (Sinha et al. 2013). The presence of loci restoring fertility for T. timopheevi cytoplasm in chromosomes belonging to homeologous groups 1 and 6 is suggested by various research groups [see Castillo et al. (2014) and references therein] and interestingly, two novel restorer loci Rf6HchS and Rf1HchS for msH1 wheat were assigned to H. chilense chromosomes 6 and 1, respectively with the former registering more effective restoration (Castillo et al. 2014). Further examination of msH1 in different genetic backgrounds led authors to substantiate that the presence of both translocation combinations 6HchS.6DL and 1HchS.1BL significantly enhanced fertility when telocentric additions 6HchS and 1HchS are already present (Castillo et al. 2015). Recently, Tsunewaki (2015) identified a 2.5 cM long segment on chromosome 1BS harboring three loci that respond to three different sterility-inducing cytoplasms i.e. Sv, T and N, and hence the genomic region was referred to as ‘‘Rfmulti’’. In Brassica, attempts aimed at mapping genetic factors that confer fertility to pol-CMS (B. napus) resulted in locating Rfp gene on LG18 (Landry et al. 1991; Jean et al. 1997; Chen et al. 2007), and the restoration ability was inherited as monogenic dominant (Liu et al. 2012a). Zhou et al. (2008) reported two AFLP-derived sequence characterized amplified region (SCAR) markers for Rfp gene. Later, Liu et al. (2012a) reported additional DNA markers [two SCARs and one simple sequence repeat (SSR)] tightly linked to Rfp gene on LG 9 of B. napus genome and notably, the mapping location agreed with the results reported earlier by Li et al. (2011). Importantly, the restorer genes Rfp (pol CMS) and Rfn (nap CMS) were mapped on the same locus in B. napus using RFLP (Li et al. 1998). The gene Rfo (extensively used in Ogura CMS) was

Plant Cell Rep

mapped on LG19 of B. napus (Hu et al. 2008; Feng et al. 2009). More recently, Rfo gene introgressed from radish was mapped on chromosome 9 of B. juncea A genome (Tian et al. 2014). Exceptionally, the genetic inheritance of fertility restorer in radish was reported to follow over dominance (Wang et al. 2013c). Recently, molecular mapping of a new monogenic dominant restorer gene Rff was performed in B. juncea, which responds to fruit CMS (Atri et al. 2016). In sorghum, two major non-allelic Rf genes influenced by some modifiers or partial fertility loci were reported in A1-CMS (Erichsen and Ross 1963; Miller and Pickett 1964; Jordan et al. 2011). The A3-CMS is rescued gametophytically by complementary interaction of two genes Rf3 and Rf4 (Tang et al. 1996, 1998; Pring et al. 1999; Wen et al. 2002; Kuhlman et al. 2006). However, recovery of fertility in 9E- and A4-CMS was accounted to sporophytic control of one or two gene(s) (Elkonin et al. 1998). Similarly, a sporophytic model in Sudangrass A3CMS described fertility by two genes showing complementary gene action (Tang et al. 2007). Notwithstanding this, A3-CMS restoration by a single gene was also envisaged (Tang and Pring 2003). Researchers while investigating fertility restoration in A1-CMS determined the position of Rf1 gene on LG8 (Klein et al. 2001; Kim et al. 2005; Klein et al. 2005). Another locus Rf2 rescuing fertility in A1-CMS was found on chromosome SBI-02 (Jordan et al. 2010). Apart from the Rf genes mentioned above, Rf5 on SBI05 conditioning complete fertility restoration along with another locus (on SBI04) recovering partial fertility in both A1- and A2-CMSs was also registered (Jordan et al. 2011). More recently, the genomic location of a novel gene (Rf6) restoring both A1-and A2-CMSs was determined on chromosome 4 (Praveen et al. 2015). To counter the sterility-inducing impact of sterile cytoplasms in sunflower, initially four Rf genes were documented depending upon the type of CMS used (Seriys 1996). To date, plenty of molecular studies have been conducted in sunflower that suggest genomic locations of different Rf genes including Rf1 (Gentzbittel et al. 1995; Jan et al. 1998; Yue et al. 2010), Msc1 (Gentzbittel et al. 1999), Rf3 (Abratti et al. 2008; Liu et al. 2012), Rf4 for CMS GIG2 (Feng and Jan 2008), Rf5 for CMS PET1 (Horn et al. 2003; Yue et al. 2010; Qi et al. 2012), Rf PEF1 (Schnable et al. 2008), Rf6 for CMS 514A (Liu et al. 2013a). As a result of these genetic analyses, the causative Rf genes were assigned to different LGs such as Rf1 on LG 6 (Gentzbittel et al. 1995), Msc1 on LG 12 (Gentzbittel et al. 1999), Rf3-RHA 340 and Rf3 RHA-280 on LG7 (Abratti et al. 2008; Liu et al. 2012), Rf4 on LG 3 (Feng and Jan 2008), Rf5 on LG13 (Qi et al. 2012) and Rf6 on LG3 (Liu et al. 2013a).

In cotton CMS-D8, two independent genes Rf1 (sporophytic restoration) and Rf2 (gametophytic restoration) contribute towards the genetic control of fertility restoration trait (Weaver and Weaver 1977; Stewart et al. 1996; Stewart and Zhang 1996; Zhang and Stewart 2001a, 2001b, 2004). Some investigators however had a proposition that CMS-D8 is rendered fertile by a single dominant Rf2 gene (Zhang and Stewart 2001a; Zhang et al. 2005). In case of CMS-D2, fertility is recovered following the action of Rf1 gene (Weaver and Weaver 1977; Kohel et al. 1984; Zhang and Stewart 2001b). Molecular evidences were also gathered supporting the view that Rf1gene operates in both CMS-D2 and CMS-D8 (Stewart and Zhang 1996; Stewart et al. 1996; Zhang and Stewart 2001a, b). Concerning chromosomal position, dominant restorer gene Rf1 was proposed to be situated on chromosome 4 (Liu et al. 2003), while Wang et al. (2009) by using a consensus mapping approach identified D5 chromosome carrying Rf1 and Rf2 as fertility rescuers for CMS-D2 and CMS-D8, respectively. In case of soybean, existence of a single Rf gene exhibiting gametophytically controlled restoration was reported (Sun et al. 2001; Zhao and Gai 2006). However, instances of sporophytically governed restoration were also encountered in soybean involving two dominant Rf genes that resume male fertility in N8855 cytoplasm (Bai and Gai 2005). More recently, a dominant Rf gene restoring ZDCMS was mapped on soybean chromosome 16 (Dong et al. 2012), and the same genomic region was earlier found responsible for imparting fertility to RN-CMS (Zhao et al. 2007) (see Supplementary Table). As speculated by authors (Dong et al. 2012), a genomic region shared between two gametophytically restored CMS (ZD and RN) implies to either a common CMS-inducing cytoplasm or a similar mechanistic explanation (a single Rf gene) for fertility restoration. The possibility of a common Rf gene restoring multiple CMSs (‘‘Pluripotential Rf locus’’ Tsunewaki 2015) in soybean is similar to what has been reported in Brassica (see Yamagishi and Bhat 2014), wheat (Tsunewaki 2015), cotton (Zhang and Stewart 2001a, b) and sorghum (Jordan et al. 2011; Praveen et al. 2015). Map based cloning of Rf genes and their functional characterization Considering the diverse ways of fertility restoration opted by Rf gene, cloning of Rf genes is imperative to gain complete understanding of the molecular mechanism underlying the CMS and fertility restoration. As shown in Table 3, conclusive findings arising from these cloning experiments have strengthened the view that most of the causal Rf genes discovered to date encode pentatricopeptide-repeat (PPR) proteins (Chase 2007; Dahan and Mireau 2013). In this regard, cloning of the restorer gene from

123

123

Rf-1 (BT- CMS)

Rice

DQ311054

Rf gene (Rf1b)

AB583700 AB583699

Rf2

(LD-CMS)

Petunia

Rf

AY102721

JX521807

JX521806

RsRf3

AY285676

AY285675

AY285674

–

Rfo (Ogura-CMS)

Radish

–

Rfk1 (Kosena-CMS)

Rf1 (NK-219 mm-CMS)

Sugarbeet

–

U43082

AB900794

AB900793

AB900792

AJ550021

Rf1 (A1-CMS)

Sorghum

F2 (WAA 9 IR24)

2423

9606H

–

D81.8

–

NK–198

RTx432

Ky2 l

–

F2 (600), 9802A1 9 9606H

–

F2 (6907) (7 ms 9 D81.8)

Two F4 populations (90, 89)

(NK–219 mm 9 NK-198)

(ATx623) 9 (RTx432)

F2 (381),

–

Rf-PPR592

–

orf687

PPR-B

–

bvORF21

bvORF19

bvORF18

bvORF20

PPR13

–

PPR782a

PPR10-454-M

AB900791

IR24

PPR7-454-M

PPR791

KJ680248

Rfo (Ogura-CMS)

rf2 (T-CMS)

Maize

Rf4 (WA-CMS)

BCF8 (1979)

LOC_Os02g17380.1

ORF11

–

Rf-1A, Rf-1B

PPR791

PPR8-1

Causative gene

PPR9-782-M

Minghui 63

LD-Akihikari 9 CSSL204

F2 (88), F3 (1500)

(CWA 9 CWR)

F2 (9184), BC (4032)

F2 (603) (731A 9 C9083)

MTC10A 9 MTC10R

BC (300),

FR Koshihikari

MS Koshihikari 9

BC (1121) (BTA 9 BTR)

Population used

KJ680249

Milyang23 KJ680250

Rf4 (WA-CMS)

Kasalath

CWR

C9083

MTC-10R

IR24

BTR

Restorer line

Rf5 (HL-CMS)

AB583698

AB481199

Rf17 (CW-CMS)

(BT-CMS)

AB112811

AB110444

AB110443

AB110016

AB106867

NCBI Accession

Rf-1 (BT-CMS)

Rf-1 (BT-CMS)

Cloned gene

Crop

Table 3 The cloned Rf loci in plants and the underlying causative genes that explain the restoration ability

PPR

PPR

PPR

PPR

PPR

Unknown

PPR

Dehydrogenase

Aldehyde

PPR

PPR

PPR

Glycine rich protein

Protein

Unknown mitochondrial

PPR

PPR

PPR

PPR

Encoded product

Bentolila et al. (2002)

Wang et al. (2013c)

Koizuka et al. (2003)

Desloire et al. (2003)

Brown et al. (2003)

Matsuhira et al. (2012)

Klein et al. (2005)

Cui et al. (1996)

Kazama and Toriyama (2014)

Tang et al. (2014)

Hu et al. (2012)

Itabashi et al. (2011)

Fuji and Toryama (2009)

Wang et al. (2006)

Akagi et al. (2004)

Komori et al. (2004)

Kazama and Toriyama (2003)

References

Plant Cell Rep

Zhu et al.(2015) – 1088 82,356 42,634,123 * Genes matching with the reference genome

Illumina HiSeq 2500 CHA-derived sterile line Wheat

Anthers

Yan et al. (2013) GSE42513 3,231 (B. rapa) and 3,371 (B. oleracea) – 2760574 (Ste) 2,714,441 (Fer) Illumina Fertile and sterile progenies B.napus

Floral buds

Yang et al.(2014) SRX547770, SRX547777, SRX547779, and SRX547781 709 (SS) 644 (MS) 86,093 206,496 Illumina HiSeq 2000 A and B lines Cotton

Floral buds

Li et al. (2015) SRP052011 365 56044* 57,382,380 (NJCMS1A) 45,599,106 (NJCMS1B) Illumina Hiseq 2000 A and B lines Soybean

Flower Buds

An et al. (2014) SRA069852 1,148 112,770 Illumina 105,481,136 HiSeq 2000 Near isogenic fertile and sterile lines B. napus

Flower Buds

NCBI accession number Differentially expressed genes Unigenes/genes Total sequences generated Platform Sample Genotypes Crop

Table 4 Next generation sequencing based transcriptome analysis of male fertile and sterile individuals to access candidate genes showing differential expression

petunia was the first report that documented PPR protein as the encoded product of Rf-PPR592 (Bentolila et al. 2002). Subsequently, positional cloning of Rf-1 gene of BT-CMS encoding PPR protein was successfully performed in rice (Kazama and Toriyama 2003; Akagi et al. 2004; Komori et al. 2004; Wang et al. 2006). However, aldehyde dehydrogenase was revealed as a translation product of rf2 gene (counteracting CMS-T) in maize instead of a PPR protein (Cui et al. 1996; Liu et al. 2001). The different mechanisms that lead to fertility restoration are discussed comprehensively in recent reviews (Dahan and Mireau 2013; Chen and Liu 2014; Hu et al. 2014). The Rf4 and Rf6 genes counteracting sterility of rice WA-CMS and HL-CMS, respectively are the recent addition to the list of cloned restorer genes. Tang et al. (2014) delineated the Rf4 locus using F2 and F5 populations (ZN 97A 9 MH 63), and they identified three candidate PPRs, of which ‘‘PPR9-782-M’’ was suggested to be the causal Rf4 based on the inferences drawn by introducing PPR9782-M segment to Jin 23 A (T0) and analysis of T1 plants (Jin 23 A 9 Jin 23 B). Further, the action of Rf4 on orf 352 (WA352) was confirmed by RNA blot analyses of an F2 population (ZSRf4 9 ZS 97B), T1 plants (Jin 23 A with PPR9-782-M) and R line (ZSRf4). The same candidate PPR named ‘‘PPR9-782a’’ was substantiated as functional Rf4 by Kazama and Toriyama (2014) via fine mapping of Rf4 locus, identification of the candidate PPRs and engineering WA-CMS line (WAA) with the candidate PPRs. In addition, the northern blots constructed for WAA, R line (WAR) and fertile transgenic plants suggested that Rf4 restores fertility in WA-CMS through enabling degradation of rpl5-orf352 transcripts. More recently, a map based cloning strategy facilitated the identification of a causative Orf 2 that underlies Rf 6 locus (Huang et al. 2015). Further investigation revealed duplication of PPR motifs (3–5), of which motif 3 is essentially required for functioning of RF 6. Unlike Rf 5 which interacts with GRP 162 to process atp6-orfH79 in HL-CMS rice, Rf 6 forms a complex with hexokinase (OsHXK6) in order to cleave the CMS-inducing transcript. Interestingly, the inability of Rf 6 and OsHXK6 to directly bind to RNA strongly points towards the involvement of additional co-factors in processing of the aberrant transcript. Similarly, participation of another element (apart from GRP 162 and RF 5) in restoration of fertility complex (RFC) that possibly cleaves the CMS transcript was also proposed by Hu et al. (2013a) who experimentally demonstrated that an artificially created Mt-GRP 162 (GRP 162 with a mitochondrial transit peptide of RF 5) restores fertility in HL-CMS via acting upon ORFH 79 instead of cleaving the atp6-orfH79 transcript. Molecular cloning of Rf genes not only refine our understanding of the cytoplasmic nuclear interactions but

References

Plant Cell Rep

123

Plant Cell Rep

also generate powerful molecular tools to underpin hybrid breeding through expediting the development of novel R lines (Kazama and Toriyama 2014).

Evolving omics technologies to decipher CMS/Rf mechanism With the current DNA sequencing techniques undergoing constant refinement in terms of quality and quantum of output, the NGS and data mining in crop species are getting extremely simplified. In this section we update the existing knowledge about CMS/Rf mechanism in view of the novel insights obtained by analyzing A, B, R and hybrids using modern omics techniques.

Whole transcriptome profiling Examining abundance of transcripts in anther or flower buds offers a potential way to decipher the causal genetic factors that play key role in the induction of male sterility as well as the retrieval of fertility. To this end, techniques like cDNA library screening/subtractive hybridization and microarray were widely used earlier to unveil the expression patterns of putative candidate genes/ORFs. For instance, a recent microarray analysis in cotton revealed a set of 458 genes differentially expressed between CMS D 8 line and its isogenic R line (Suzuki et al. 2013). Majority of which, as illustrated by the functional categorization, were found to be contributing in cell wall expansion. Huang et al. (2011) have reviewed anther transcriptome analyses primarily cDNA libraries/microarray in various crops. In recent years, conventional methods of transcript profiling have been increasingly replaced by modern NGS techniques like RNA-seq given its high-throughput nature to pinpoint critical gene(s) (Mantione et al. 2014). Recent comparative transcriptome studies have focused on identifying the genes that specify the CMS and fertility restoration (Table 4). It is important to note here that these global gene expression analyses concentrated primarily on isogenic lines that share identical sterile cytoplasm. For instance, Yan et al. (2013) uncovered a set of differentially expressed genes (DEGs) in B. napus by analyzing transcriptomes of fertile and sterile plants from F1s (Nsa CMS 9 NR 1). The DEGs belonged to the genome donors i.e. B. rapa (3231) and B. oleracea (3371). Interestingly, the study generated unique sequence tags that were supposed to represent the genomic fraction received from Sinapis arvensis. Given the complete absence of these tags in sterile individuals, these unmatched sequence tags open novel avenues for capturing fertility determinants. Similarly, RNA seq of fertile and sterile floral buds from B.

123

napus isogenic lines provided a set of 1148 DEGs between fertile and sterile pools (An et al. 2014). Based on the GO and KEGG analyses, authors proposed that a defective atp 6 structure could result from co-transcription of orf-224 and atp 6, causing impairment in the usual ATP production. Counteracting on orf-224/atp 6, nucleus encoded Rfp gene, however, facilitates re-formation of functional ATPase protein 6, which subsequent leads to fertility restoration. Since pollen being a ‘‘non-photosynthetic system’’ relies entirely upon mitochondrial function to cater its enhanced energy needs (Selinski and Scheibe 2014), the energy deficiency has been proposed as an obvious reason to comprehend the phenomenon of male sterility in plants (see Chen and Liu 2014). The proton gradient generated through electrons flowing across electron transport chain (ETC) (Complex I–IV) is harnessed by the ATP synthase in order to produce energy. Further, mutations in some genes encoding respiratory chain proteins have been reported to cause male sterility (Rasmusson et al. 1998; Chase and Gabay-Laughnan 2004). Evidences associating the ETC impairment with CMS emanate from treating plants with chemicals that inhibit the ETC (see Yamagishi and Bhat 2014). However, Touzet and Meyer (2014) by citing exceptional OXPHOS mutants (able to produce fertile pollens despite having defective ATP production system) contested this long-established view that CMS only arises owing to the ATP related deficiencies in plants. Similarly, Yang et al. (2014) using RNA expression data envisaged that the reduced ATP production might not be the sole cause for sterility in cotton. Taken together, these crucial findings serve to refine our understanding about CMS in relation to disrupted mitochondrial ATP synthesis. Yang et al. (2014) found 707 and 644 DEGs to be significant in JA CMS line at sporogenous cell (SS) stage and microsporocyte (MS) stage, respectively. Moreover, 17 and 38 genes showed differential expression, respectively in JACMS and JB while comparing the two stages within individual line. Precisely, genes related to events like ‘‘redox reaction’’ and ‘‘alfa linolenic acid metabolism’’ were found to be down-regulated in contrast to the ‘‘photosynthesis’’ and ‘‘flavonoid biosynthesis’’ related genes which exhibited up-regulation. As a testimony to the contribution of flavonoids towards pollen development, flavonoid deficient mutants in maize and petunia lacking chalcone synthase (a key enzyme in flavonoid biosynthesis pathway) were found incapable of producing a functional pollen tube (Yan et al. 2013). By contrast, Ylstra et al. (1996) observed no such pollen tube aberration in Arabidopsis while examining the impact of flavonol (resulting from mutated chalcone synthase gene) on fertilization. A recent study involving lap mutants (LAP 5/6) in Arabidopsis deduced that a reduction in flavonoid content could be credited to the disturbance in pollen exine

Plant Cell Rep

deposition as a result of which male sterility is manifested (Kim et al. 2010; Ferreyra et al. 2012). More recently, a set of down-regulated genes pertaining to the reactive oxygen species (ROS) scavenging (15), calmodulin (12) pollen wall formation (34) and transcription factors (14) was reported in soybean A line (Li et al. 2015). Notably, up-regulation of one gene ‘‘aspartic proteinase A100 in the A line helped authors to draw meaningful correspondence between the programmed cell death (PCD) and the CMS phenotype. Further, DEGs engaged in carbohydrate and energy metabolism provided evidences in support of greater energy demand and reduced supply leading to sterility. Earlier researchers while working on rice CMS-HL (Peng et al. 2010; Wang et al. 2013b) reported that reduced ATP/ADP ratio, lower respiration rate and oxidative burst influenced the development of not only the male gametophyte but also the root. Likewise in the CMS WA rice, the PCD and eventual pollen abortion are caused by an impaired functioning of COX11 resulting from an interaction between the mitochondrial gene (WA352) and the COX11 (Luo et al. 2013). In the context, release of cytochrome c and overproduction of the ROS constitute crucial events that eventually facilitate the PCD (Gill and Tuteja 2010). However, Touzet and Meyer (2014) referred to the case of respiratory mutants in which enhanced ROS production remained inadequate to elucidate the phenomenon of pollen sterility. Also, exciting avenues are opened in recent times for combining the omics data with cellular-level description to generate a high-resolution landscape of gene expression and network. For instance, a 44 K microarray based transcriptome profiling of the laser microdissection (LM) separated microspores/pollen and tapetum in rice by Suwabe et al. (2008) not only corroborated with the previous findings but additionally made an unambiguous distinction between the pollen and tapetum specific genes which were classified in earlier studies collectively under the anther transcriptome. This LM-Microarray technique was intensively used in rice for the identification of candidate genes playing important roles in development of sporophytic tissue and the male gemetophyte (Hobo et al. 2008; Aya et al. 2011). For further details the reader is referred to the reviews published on cell type specific transcriptome sequencing (Ohtsu et al. 2007; Rutley and Twell 2015). In addition to the crops selected herein for discussion, RNA Seq-transcriptome profiling of CMS was published recently in chili pepper (Liu et al. 2013b), garlic (ShemeshMayer et al. 2015) and the technique is likely to be extended to other important crops with CMS, especially the lesser studied crops like pearl millet that currently lack a reference genome sequence.

Whole genome sequencing of mitochondria Known as the powerhouse of the cell, mitochondria show highly variable sizes ranging from 100 to 11,000 kb in plants than reported in case of animals (*16 kb) (see Tuteja et al. 2013). Extensive genomic reorganizations occurring largely in the non-coding regions are considered as the prime driving force that shapes the plant mitochondrial genomes and is also known to induce sterile phenotypes (Horn et al. 2014; Tan et al. 2015). The bigger mitochondrial size of A lines in comparison to their cognate B lines is credited to the repeat elements in the noncoding reasons (Liu et al. 2011). Therefore, in view of the significant contribution of mitochondria towards the CMS, substantial attempts were made to sequence the entire mitochondrial genomes of A, B and R lines (Table 5). To this end, technical advances in sequencing chemistry have led researchers to increasingly access the entire mitochondrial genomes. And eventually, a detailed comparison with the reference mitochondrial genome has facilitated uncovering of several novel orfs which could help greatly to illuminate the hitherto elusive mechanism of sterility and fertility restoration in plants. Once the whole mitochondrial sequence is established, a candidate CMS orf is searched targeting a particular genomic region in mitochondrion that (1) remains restricted to CMS plants, (2) displays a chimerical structure neighboring essential genes and (3) translates into peptides with membrane spanning domains (Fujii and Toriyama 2008; Kubo et al. 2011; Igarashi et al. 2013; Okazaki et al. 2013; Heng et al. 2014). Okazaki et al. (2013) sequenced mitochondrial genomes of A line (RT 102 A), R line (RT 102 C) and Nipponbare, and based on the parameters described above they discovered a novel orf gene (orf352) in RT 102 CMS rice. Applying the same criteria, six orfs (orf340, orf276, orf210, orf174, orf83a and orf113) were identified as candidates for CMS in rice RT 98 (Igarashi et al. 2013). Of these, only a single orf (orf113) could generate differential expression patterns between A and R lines in Northern blot analysis, thereby revealing its contribution to CMS manifestation in RT 98. Clearly absent from Nipponbare mitochondrial genome, orf113 was co-transcribed with atp4 and cox3 genes. A recent investigation on 454-sequenced mitochondrial genomes of hau CMS, its maintainer and B. juncea normal type uncovered a chimeric orf288 gene cotranscribed with atp6 (situated upstream). Further, DNA markers (SCARs) developed from orfs exclusive to A (orf235, orf170 and orf288) and B (orf109, orf293 and rps7) lines effectively discriminated the two lines at early growth stages. However, amplification of some SCAR markers in both lines (A and B) could be seen as striking evidence to support the view that ‘‘substoichiometrically different mitotypes’’ coexist in B. juncea (Heng et al.

123

123

A1 CMS

Sorghum

NxSeq

454 FLX

454 FLX?

hau CMS line, B-line and normal (J163-4)

ICPA 2039, ICPB 2039, ICPH 2433

–

ABI

Male-fertile inbred B37 N

pol-CMS line NH12A

–

CMS-T, CMS-C, and CMS-S, A188 (NA)

Pigeonpea

Brassica napus Brassica juncea

Maize

ABI3730

K-type B line (Yumai 3)

454 GS FLX

WA-CMS

ABI3730xl

454 GSFLX

RT102A CMS line

K-type CMS line

454 GSFLX

RT98A CMS line

Wheat

454 GSFLX

LD-CMS, CW-CMS

Rice

Platform

Genotypes

Crop

Circular

Circular

Circular (tripartite) Circular

Circular

Circular

Circular

Circular

Circular

Circular

Circular

Circular

Shape

454

545.7

247.9, 219.8 (B line and Normal)

223

569.6

535. 8 (CMS-T), 557.1 (CMS-S), 701 (NA), 739.7 (CMSC)

452.5

647.5

401.5

502.2

525.9

434.7 (LD-CMS), 559 (CWCMS)

Size (Kbp)

–

51

35-36

55

58

51

35

34

–

–

–

54

Genes/Protein coding genes

–

13 chimeric orfs

orf122 and orf132 (pol-specific) orf288

orf186 and orf127

Several orfs for CMS-S and CMST

–

22 unique ORFs, missing rpl5

orf126

orf352

orf 113

orf307

Candidate orfs

–

SRA053693

KF736092 (A-line), KF736093 (B-line)

FR715249

AY506529

DQ490951 (CMS-S), DQ490952 (NA), DQ490953 (CMS-T), and DQ645536 (CMS-C)

EU534409

GU985444

JF281154

AP012528

AP012527

AP011076 (CW-CMS), AP011077 (LD-CMS)

Accession number (NCBI/ EMBL)

Table 5 The male sterility inducing loci in different crops as revealed by the high-throughput sequencing of whole mitochondrial genome of fertile and sterile lines

Klein et al. (2015)

Tuteja et al. (2013)

Chen et al. (2011) Heng et al. (2014)

Clifton et al. (2004)

Allen et al. (2007)

Cui et al. (2009)

Liu et al. (2011)

Bentolila and Stefanov (2012)

Okazaki et al. (2013)

Igarashi et al. (2013)

Fujii et al. (2010)

References

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Plant Cell Rep

2014). A similar analysis using mitotype-specific DNA markers suggested simultaneous occurrence of different mitotypes (pol and nap) at substoichiometric scale in B. napus (Chen et al. 2011). As a result of co-existence of pol and nap mitotypes, ratios of orfs i.e. orf 224/orf 222 and orf 222/orf 224 were reported to vary in pol and nap cytoplasms, respectively. The sequence comparison between nap and pol mitotypes revealed two orfs exclusive to pol CMS while sequence variation was noted for other two orfs. The fate of the two unique orfs remains to be seen (Chen et al. 2011). Nevertheless, these findings led authors to consider substoichiometric shifting as a potential event leading to the CMS diversification. In rice, a comparative analysis of whole mitochondrial sequences of CW-CMS and LD-CMS using Nipponbare as reference shed light on the evolutionary aspects of the CMS-associated genes with authors concluding that modern breeding practices have substantially influenced the CMS-associated factors including the removal of some known orfs like orf 307 (CW-CMS) and orf 79 (LD-CMS) and the creation of some novel orfs. A robust explanation for the novel orf 288 inducing sterility in CW-CMS, however, could not be served (Fujii et al. 2010). Likewise, sequence comparison between KS3 (A line derived from A. kotschyi) and Km3 (B line: Triticum aestivum Yumai 3) mitochondria in wheat illustrated 22 ORFs unique to sterile line (Liu et al. 2011). Besides notable absence of ribosomal protein gene (rpl5), genes related to respiratory chain like atp6, nad9 and nad6 also showed pronounced differences in case of A line. The 454 sequencing was also employed in pigeonpea to sequence mitochondrial genomes of A4 cytoplasm based A-line, B-line, hybrid and wild progenitor Cajanus cajanifolius (Table 5). Conclusively, 13 chimeric orfs (associated with genes including cox3, nad7, mttB and ccmFc) were proposed to be the putative candidates for conditioning sterility in A4 cytoplasm (Tuteja et al. 2013). Importantly, to experimentally validate these newly searched CMS-associated orfs, the counter-action of the Rf genes is examined on the expression patterns of these orfs (Okazaki et al. 2013). In other words, given that these orfs are co-transcribed with other mitochondrial genes, the resultant transcripts might be acted upon by the proteins encoded by Rf genes and this interaction in turn resumes fertility (Horn et al. 2014; Hu et al. 2014). For instance, suppressed expression of rpl5-orf 352 (cleaved transcript) in the presence of Rf 102 gene supported the proposition that orf 352 induces sterility in RT 102 CMS rice (Okazaki et al. 2013).

increasingly underscored in recent times (Millar and Gubler 2005; Wu et al. 2006; Wei et al. 2013). Enhancements in NGS have introduced new methods that allow mining and expression study of miRNAs at unprecedented scale (Li et al. 2010). More importantly, the data are made accessible to the research community in the form of an online repository, for example miRBase (the microRNA database: www.mirbase.org) (Griffiths-Jones 2006). Further, to functionally confirm the identified miRNAs, computational predictions and 50 -rapid amplification of cDNA ends (RACE) are the methods often employed for mRNA targets to be identified and validated (Watanabe et al. 2007). Notwithstanding the widespread acceptance, validation of mRNA targets using RACE assay remains a daunting task given its reliance on individual mRNA degradation fragments (Li et al. 2010; Yan et al. 2015). To address the issue described above, comprehensive survey of ‘RNA targets’ is effectively done by NGS-driven degradome sequencing or parallel analysis of RNA ends (PARE) as demonstrated in Arabidopsis and rice (German et al. 2008, 2009; Li et al. 2010; Zhou et al. 2010). A set of 290 new candidate miRNAs was discovered between B. juncea A and B lines. This was accompanied by a degradome analysis, which uncovered more than 700 mRNA targets. Among which, the BjAPS1 (target gene for miR395a) reflected its greater abundance in A-line than B-line when analyzed by q-PCR. And notably, the expression was further elevated in floral buds treated with oligomycin (an inhibitor of ATP synthase), pointing to a possible link between miRNA, retrograde signaling and the CMS (Yang et al. 2013). Similarly, prediction of targets for 24 miRNA expressed differentially between ZD-CMS MxA and MxB in rice enabled authors to associate these ‘negative regulators’ with the CMS occurrence (Yan et al. 2015). More recently, Illumina sequencing of small RNA libraries of NJCMS1A and its maintainer NJCMS1B in soybean revealed miRNAs that are predicted to be associated with impairments caused during the development of male gametophyte. By associating differential expressions of miRNAs with their corresponding mRNA targets in the two lines, authors suggested engagement of these noncoding molecules with PPR, ROS, PCD and ATP deficiency (Ding et al. 2016). Involvement of non-coding RNAs (ncRNAs) in regulating the mitochondrial mechanism was proposed in rice based on mitochondrial transcript profiling (Fujii et al. 2011). Investigating proteomes for greater insights

High throughput sequencing and degradome analysis to elucidate the role of miRNA Contribution of miRNAs (*22 nucleotide non-coding RNA molecules) to male and female reproduction has been

In some instances, transcript abundance may not show significant difference between fertile and sterile plants, however differential expression patterns exist at protein level (Hu et al. 2013b). This implies towards a need to

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investigate proteomes to allow a comprehensive understanding of the CMS/Rf phenomenon (Chen and Liu 2014). In HL CMS rice, two-dimensional electrophoresis (2DE) applied in anthers of Yuetai A, Yuetai B and F1 (HonglianYou 6: Yuetai A 9 9311) produced 48 differential protein spots, which were subsequently confirmed by mass spectrometry (MS). Functionally categorization of these proteins linked them with cellular processes responsible for development of pollen grains (Wen et al. 2007). Similarly, anther proteins from Yuetai A, Yuetai B and F1 were later analyzed with isotope-code affinity tag (ICAT) technology, based on which a set of 97 unique proteins was recovered (Sun et al. 2009). These studies underlined the relevance of proteins related to energy production machinery in generating sterile phenotypes in HL-CMS rice (see Wang et al. 2013a). More recently, over 600 proteins were quantified in ZD-CMS A (Meixiang A) and B (Meixiang B) applying isobaric tags for relative and absolute quantitation (iTRAQ) assay (Yan et al. 2014). Further, functions were assigned to 45 proteins that showed greater than 10 % fold change. Majority of these proteins were noted to be engaged with protein (9) and carbohydrate (8) metabolism, and stress response (8). With respect to the mitochondrionlocated proteins, six differentially expressed proteins included lactate/malate dehydrogenase (MDH) (carbohydrate metabolism), heat shock protein 90 (Hsp90) and aldehyde dehydrogenase (ALDH) (stress response), inorganic H? pyrophosphatase, phosphate carrier protein (transporters), calreticulin precursor protein (CRT) (Ca?? signaling). Further, iTRAQ assay was accompanied by qPCR (7 genes) and western blot (3 proteins) to gather confirmatory evidences. Importantly, the differences observed between the patterns of transcriptome and proteome profiles from the same tissue of a given genotype warrants integrating the multiple layer of information originating from different omics platforms. For example, in garlic, Shemesh-Mayer et al. (2015) dramatically reduced the number of candidate genes by combining the transcriptomic, quantitative PCR and proteomic data, and they ultimately extracted two robust candidate genes flavanol synthase and superoxide dismutase (SOD) to be expressed exclusively in the A-line i.e. MS 96. Importantly, authors noted only one transcript out of the six transcripts mapped to ADP-ribosylation factor 1 (which showed specific accumulation in MS 96) which could differ significantly between the fertile and sterile lines. This study supported the view that considers deregulated PCD, the ROS trigger and inadequate ATP supply as the key reasons for male sterility in plants. Specifically, mitochondrial proteome can be profiled to comprehend the CMS/Rf mechanism. Recently, blue-native (BN)/SDS-PAGE, 2DE, in-gel activity assay and MS

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enabled the identification of mitochondrial proteins in sugar beet exhibiting qualitative and quantitative abundance between A, B and R lines (Wesołowski et al. 2015). Abundant proteins included preSatp6, HSP60, glutathione reductase (GR), and ATP9 in sterile lines and MnSOD in fertile lines. Along with highlighting the quantitative difference of ATP9 protein between mitochondrial proteomes of A and B/R lines, authors suggested that preSatp6 and Rf1(X) interact with ATP9 to cause the ROS generation and fertility restoration, respectively.

Marker assisted selection (MAS) to accelerate CMS-hybrid breeding Rapid discovery of potential restorers from a wider germplasm set, precise introgression of Rf-containing chromosomal segments to diverse genetic backgrounds, rapid discrimination among parental lines, and ensuring the genetic purity (parents/hybrids) constitute crucial steps in CMS-based hybrid breeding. Success of any CMS-hybrid breeding programme hinges upon the constant supply of genetically pure seeds of parental lines (Sattari et al. 2007; Sundaram et al. 2008; Saxena et al. 2010b; Qi et al. 2012; Bohra et al. 2012, 2015). Notable studies have been published that underline the immense relevance of MAS while tracking the introgression/transfer of desirable genomic segment, and a variety of DNA markers associated with Rf genes were employed in MAS scheme to enable fast-track recovery of potential R lines (carrying the relevant Rf gene) for diverse sterile cytoplasms. Examples include SSRs in HL-CMS (Huang et al. 2003), WA-CMS (Jiang et al. 2001; Ahmadikhah and Karlov 2006; Ngangkham et al. 2010; Suresh et al. 2012) and CW-CMS (Fujii and Toriyama 2005); two YAC-based probes in CMS-WA (Zhang et al. 2002) and cleaved amplified polymorphic sequence (CAPS) markers in CMS- CW (Fujii and Toriyama 2005). Besides exploring R-lines, DNA marker technology offers advantage of early discrimination among parental lines e.g., RAPD (Sane et al. 1997; Ichii et al. 2003), SSR (Sheeba et al. 2009) and CAPS (Ngangkham et al. 2010). Notably, the DNA markers for Rf3 and Rf4 genes were found to be effective in hybrid rice breeding not only to detect the relevant Rf fragments but also for pyramiding Rf genes into better agronomic bases (Sattari et al. 2007). The enhanced scope for obtaining desirable combinations of Rfgenes into novel R-lines was shown by pyramiding multiple Rf genes using SSR markers (Bazrkar et al. 2008). More recently, Ahmadikhah et al. (2015) demonstrated fast-track conversion of rice CMS line by applying marker assisted backcrossing (MABC) technique with SSR and inter simple sequence repeat (ISSR) markers, thereby successfully converting a B-line (Yosen B) into A-line.

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Similarly in maize, the RFLPs facilitated screening of rf1 and rf2 genes for T- CMS (Wise and Schnable 1994), whereas linkage of CAPSE3P1 and SCARE12M7 was established with Rf3 gene for S-CMS (Zhang et al. 2006). In wheat, RFLPs (associated with genes Rf4 and Rf3) could be implemented in timopheevi-based hybrid programme (Ma and Sorrells 1995; Kojima et al. 1997), while SCAR and SSR markers could prove useful in extracting restorer gene D2Rf1 acting on D2-type CMS wheat (Li et al. 2005). Recently, the diverse CMS lines derived from Aegilops kotschyi, Ae. ventricosa and T. spelta were successfully discriminated when analyzed with AFLP technology (Ejaz et al. 2013; Zhu et al. 2013). MAS using Rfl gene-linked RAPDs was demonstrated in Brassica hybrid breeding (Janeja et al. 2003b). Further, linkage of AFLP marker with Rft1 restorer gene was harnessed to identify potential restorers for Brassica CMS programme (Janeja et al. 2003a). A set of DNA markers comprising five from B. napus and four from radish were employed recently to screen R-lines in B. juncea hybrid scheme (Tian et al. 2014). Further, the authors reported effective DNA markers (N12905, ScH03 and BolJon) in B. juncea to obtain Rf0-containing line (VR441) with improved agronomic performance. More recently, utility of the Rf gene-associated DNA markers (BjESSR01 and BjEST01) in relation to B. juncea hybrid breeding programme was also discussed (Bisht et al. 2015). Klein et al. (2001) proposed that the AFLP technology could be potentially used for screening Rf1-contaning R-lines in A1 CMS-based hybrid breeding in sorghum. Also, the STS/CAPS markers could be of greater use while identifying R-lines in sorghum that carry rf4 gene (Wen et al. 2002). Similarly, the Rf2 locus linked with Xtxp304 SSR marker makes it a good candidate region for downstream applications (Jordan et al. 2010). Recently, feasibility of SSR markers for detecting Rf6 gene (restoring fertility in A2 and A1 CMS) was explored (Praveen et al. 2015). In sunflower, robust predictive DNA markers enabling differentiation/development of R-lines and precise incorporation of Rf-containing genomic segments include AFLPs (Kusterer et al. 2005, Schnabel et al. 2008), SSRs (Feng and Jan 2008; Qi et al. 2012; Liu et al. 2012, 2013a), SCAR (Horn et al. 2003; Anisimova et al. 2011), and target region amplified polymorphism (TRAP) (Yue et al. 2010). More interestingly, while mapping rust resistant locus R11, SSR marker (ORS728) was found to show linkage with genes Rf5 and R11 (Qi et al. 2012). Availability of such DNA markers paves the way for multiple trait improvement, which still remains strenuous with conventional breeding protocols. The utility of CAPS, AFLP and SSR markers (linked with the Rf2 gene) is worth noting while addressing restoration issues in CMS-D8 cotton (Wang et al. 2007).

Recently developed CAPS-R marker (based on PPR candidate gene) associated with Rf1 gene could be chosen for surveying germplasm to detect restoration sources that contain Rf1 (Wu et al. 2014). Additionally, the authors also suggested that SSR marker (BNL3535) mapped at 0.049 cM with Rf1 gene could be an excellent candidate DNA marker for exercising MAS. Likewise, a TRAP marker (0.8 cM from Rf1 gene) was found to be associated with the genomic region responsible for conferring fertility in CMS-D2, whereas linkage of SSR markers with Rf2 gene could play a larger role in distinguishing R lines used in CMS-D8 hybrid programme (Wang et al. 2009). Likewise, the SSR markers closely associated with the Rf genes provide the opportunity to expand the array of R-lines in soybean (Yang et al. 2007; Wang et al. 2010a; Dong et al. 2012). With dramatic advancement in marker technology, new generation of markers such as DNA methylation specific epigenetic marker has been introduced that is able to explore variation existing beyond the nucleotide sequence level (Bird 2007). To this end, methylation-sensitive amplification polymorphism (MSAP) technology was recently implicated in wheat to analyze A and B lines belonging to diverse cytoplasms i.e. K, T and S (Ba et al. 2015). Marked variation comprising hypermetylation/demethylation inferred from this study underscores the enormous potential of epigenetics in resolving the CMS mechanism and to aid hybrid breeding in field crops. Recognizing the crucial role of mitochondrial genome in male sterility, creation of mitochondrion derived DNA markers has received considerable attention among scientists engaged in CMS related research. Mitochondrial sequence specific markers were employed to reveal genomic differences between WA CMS lines and their B-lines in rice (Yashitola et al. 2004; Rajendrakumar et al. 2007). Rajendrakumar et al. (2007) also highlighted the wider scope of DNA markers in establishing distinctiveness between A- and B-lines derived from O. nivara and O. rufipogon. A recent study in rice reported a novel chimeric sequence L-sp1 from mitochondrion, which based on comparative sequence analysis was found to strikingly differ from the earlier known ORFs i.e. orfH79 and WA352. Furthermore, a backcross scheme assisted by sequence specific primers led to the development of new sterile lines characteristically carrying L-sp1 sequence (Tan et al. 2015). Similarly, by targeting the length variation [between A (ICPA 2039) and B (ICPB 2039) lines] in the nad7a region of nad7 gene, an indel marker (nad7a_del) was developed in pigeonpea and the marker successfully differentiated A and B lines belonging to A4 cytoplasm. The nad7 gene was chosen based on its differential expression pattern between ICPA 2039 and ICPB 2039 (Sinha et al. 2015). The same research group has

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developed a set of 24 mitochondrial SSR markers which could be a valuable genomic resource to underpin CMS hybrid breeding in pigeonpea (Khera et al. 2015). In cotton, distinction between CMS-D8, CMS-D2 and A1 CMS lines was established through mitochondrial genes viz. atp1 and atp6 employed as RFLPs (Wang et al. 2010b). Likewise, probes specific to three mitochondrial gene cox3, atpA, and nad6 were successfully utilized as RFLP markers in distinguishing CMS-D2 lines in cotton (Wu et al. 2011). In soybean, amplicon pertaining to the ISSR marker (ISSR829) obtained by screening mitochondrial DNA was sequenced to SCAR which showed variation between A and B lines (Zhang et al. 2012). Besides mitochondrion, chloroplast was also targeted to uncover sequence variants between A and B lines. Examples include complete chloroplast sequencing of A line (JLCMS9A) and its cognate B line (JLCMS9B) in soybean, and the sequence variation (single nucleotide polymorphism: SNP) between the two lines facilitated development of a set of four DNA markers (RE1-RE4) producing promising results when employed on RN-type A and B lines (Lin et al. 2014). Materially inherited nature of chloroplasts like mitochondria renders them attractive for the development of diagnostic DNA markers (Lin et al. 2014). In addition, miscellaneous applications of DNA markers in CMS-based hybrid breeding involve their extensive use in construction of high heterotic groups, for example to permit generation of superior hybrids in rice (Xie et al. 2013). Genetic purity of the hybrid was assessed through conducting SSR assays in pigeonpea (Saxena et al. 2010b) and sorghum (Arya et al. 2014). Keeping in view the huge economic loss incurred in hybrid breeding by the impure seeds (Yuan 1985), ensuring genetic purity of component lines and hybrids in CMS system using molecular tools offers tremendous benefits in terms of time, money and labour (Bohra et al. 2015).

Perspectives Remarkable research milestones were met in recent years to elucidate the complex mechanisms that control compatibility reactions between the cytoplasmic and nuclear genomes in plants. Concurrent with the discovery of novel sterility-inducing orfs, fine mapping of the candidate genomic segment has facilitated positional cloning and functional characterization of the causative Rf genes in various crops. The experimental conclusions arising from different studies collectively led to the establishment of models that profoundly explain the phenomena of CMS and fertility restoration in crop plants (Chen and Liu 2014). The existing knowledge about the regulatory mechanism of

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CMS/Rf is likely to enrich with the increasing application of modern omics tools and technologies. To this end, analyzing mitochondrial genome, transcriptome and proteome holds greater relevance. Equally important will be the magnitude of efforts directed to harness the extensive omics data accessible through several community-oriented repositories. Besides, large-scale phenotyping protocols demand innovation not only to efficiently extract potential restoration sources from a wider germplasm pool but also for the precise evaluation of the traits that are relevant for efficient hybrid seed production (Langer et al. 2014). Concomitantly, the focus should also be on diversification of stable CMS sources and their associated Rf sources (Serieys 1996). In the context, the modern genomic tools have the potential to greatly accelerate CMS-based hybrid breeding via rapid development of new elite A, B and R lines. In addition, DNA marker technology may facilitate speedy incorporation of novel traits into parental lines and these traits can subsequently be stacked in the derived hybrids (Zhou et al. 2003; Zhan et al. 2012; Jiang et al. 2012). Genomics assisted schemes should concentrate on improving genetic resources that can be used by a broader community; for instance new traits may be introduced into the lines which contribute hybrids having widespread acceptance. Furthermore, diagnostic DNA markers that can precisely discriminate between the parental lines and hybrids can ensure their genetic purity, thereby supplementing the conventional grow-out-test (GoT) in hybrid breeding scheme (Rajendrakumar et al. 2007; Saxena et al. 2010b). Deployment of genome-scale techniques like GWAS will help illuminate the genetic landscape of fertility restoration trait with enhanced resolution (Feng et al. 2015). Further, as demonstrated recently in wheat implementation of genome-based predictions for improving hybrid performance could witness notable achievements such as sustained gains resulting from heterotic group construction (Zhao et al. 2015), and the genomic selection becomes particularly relevant in case of relatively low or ‘‘realistic’’ prediction accuracies (Longin et al. 2015). To sustainably feed over 12 billion people that are likely to populate the earth by the end of 21st century (Gerland et al. 2014), the accelerated hybrid breeding of field crops offers a way to attain the projected targets in global food production. However, according to Longin et al. (2014) a set of factors including long-term yield advantage, ‘‘variance components’’ and importantly, the cost-effectiveness of the seed production technique will potentially motivate crop breeders in future while making a choice for hybrid breeding. Authors’ contribution statement AB conceived the idea and wrote the manuscript. AB, UCJ and PA conducted literature reviews. DB and NPS contributed to the draft of

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the manuscript and edited manuscript with AB. All authors read and approved the final manuscript. Acknowledgments Authors acknowledge support from Indian Council of Agricultural Research (ICAR), India. Compliance with ethical standrads Conflict of interest The authors declare that they have no conflicts of interest.

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