PLANT SIGNALING & BEHAVIOR 2016, VOL. 11, NO. 3, e1136764 (6 pages) http://dx.doi.org/10.1080/15592324.2015.1136764
MINI-REVIEW
ATP binding cassette G transporters and plant male reproduction Guochao Zhaoa, Jianxin Shia, Wanqi Lianga, and Dabing Zhanga,b a
Joint International Research Laboratory of Metabolic & Developmental Sciences, Shanghai Jiao Tong University (SJTU)-University of Adelaide Joint Center for Agriculture and Health, State Key Laboratory of Hybrid Rice, School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai, China; bSchool of Agriculture, Food, and Wine, University of Adelaide, Urrbrae, South Australia, Australia
ABSTRACT
ARTICLE HISTORY
The function of ATP Binding Cassette G (ABCG) transporters in the regulation of plant vegetative organs development has been well characterized in various plant species. In contrast, their function in reproductive development particularly male reproductive development received considerably less attention till some ABCG transporters was reported to be associated with anther and pollen wall development in Arabidopsis thaliana and rice (Oryza sativa) during the past decade. This mini-review summarizes current knowledge of ABCG transporters regarding to their roles in male reproduction and underlying genetic and biochemical mechanisms, which makes it evident that ABCG transporters represent one of those conserved and divergent components closely related to male reproduction in plants. This mini-review also discusses the current challenges and future perspectives in this particular field.
Received 9 December 2015 Accepted 22 December 2015
Lipids and their derivatives, such as fatty acids and phospholipids are important structural components of the plant reproductive organs, therefore lipid metabolism plays important roles in plant reproduction.1 Similar to plant vegetative organs, the reproductive organ anther is also covered by a protective layer called cuticle, consisting mainly of lipid derived waxes and cutin components, which safeguards the normal development of the male gametophyte.2,3 The mature pollen has typical 3 wall structures (the outer exine, the inner intine, and the tryphine), which protects male gametophytes and facilitates male gamete survival and pollination (pistil-stigma interaction, pollen germination and hydration).1 The molecular mechanisms underlying the biosynthesis and modification of various lipidic precursors for anther cuticle and pollen wall formation in plant reproductive organs have been revealed via multiple approaches.1,4 Those studies highlight the coordinated function of sporophyte (tapetum) and gametocyte (pollen) in the process, and pinpoint the indispensable role of lipid transport in this process1,5 ATP Binding Cassette G (ABCG) transporters, comprising the half-size white/brown complex (WBC) transporters and the full-size pleiotropic drug resistance (PDR) subgroup members, are markedly expanded in plants, with more than 40 members in both Arabidopsis and rice.6 Although plant WBCs and PDRs are phylogenetically separated, both are associated with taxon-specific functional diversification, including plant defense and cuticle formation.6 In this mini-review, we focus mainly on those ABCG transporters in the context of their functions in male production, which is obviously functionally
CONTACT Dabing Zhang © 2016 Taylor & Francis Group, LLC
[email protected]
KEYWORDS
Anther cuticle; dimerization; male reproduction; pollen wall; sporopollenin
conserved at least between dicot Arabidopsis and monocot rice (Table 1). In past 2 decades, ABCG transporters in many plant species were identified to be involved in the cuticle secretion, transporting lipid molecules (precursors of wax, cutin and/or suberin) to across the plasma membrane to the epidermis. In Arabidopsis, the reported ones included AtABCG1, AtABCG2, AtABCG6, AtABCG16 and AtABCG20,7 AtABCG11,8,9 AtABCG12,10 AtABCG13,11 AtABCG9 and AtABCG31,12 AtABCG14,13-15 AtABCG26,16-18 AtABCG29,19 AtABCG32.20 In rice, the reported ABCG proteins were OsABCG15/ PDA1,21,22 OsABCG2623 and OsABCG31.24 Other reported ABCG proteins included Physco mitrella patens Pp-ABCG7,25 potato ABCG126 and barley HvABCG31.24 However, loss-offunction of some ABCG transporters affected profoundly plant development, particularly male reproductive organ development, leading to partial or complete sterile.11,16,21-23,27,28 It is worthy to note that most of the male reproduction associated ABCG transporters are half-size WBCs, although one full-size PDR, ABCG32/PEC1 (together with its ortholog in barley HvABCG31 and rice OsABCG31) also affects floral organ development.24,29
ABCG transporters and pollen wall development ABCG transporters play important roles in the allocation of various lipidic, phenolic, and other sporopollenin precursors and tryphine components from the tapetum where they are generated to the anther locule for pollen wall formation.1
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Table 1. ABCG transporters involved in the reproductive organs development. Gene name in Arabidopisis
Gene name in rice
Gene name in other species Pp-ABCG7
AtABG11
OsABCG26
AtABCG26
OsABCG15
AtABCG9 and AtABCG31 AtABCG1 and AtABCG16
Function Moss Physcomitrella patens Pp-ABCG7 affects spore wall architecture AtABG11 is involved in the formation of the cuticular barriers in both vegetative and reproductive organs. OsABCG26 is mainly responsible for the export of tapetum generated lipid precursors for anther cuticle formation. Both are involved in the transfer of sporopollenin precursors from tapetal cells to anther locules, facilitating exine formation These 2 genes collaboratively transfer tryphine components from tapetal cells to anther locules for tryphine deposition These 2 genes collaboratively transport nexine precursors from tapetal cells to anther locules and transport intine precursors across microspores plasma membrane for intine development
Arabidopsis AtABCG26 is responsible for the transport of polyketides for exine formation, and loss-of-function of ABCG26 results in significantly reduced fertility.16-18,30 atabcg26 mutant tapetal cells accumulate numerous electron-lucent vesicles and numerous electron-dense granules, and display accumulated large fluorescent vacuoles in tapetal cells with corresponding loss of fluorescence on microspores as evidenced by 2 photon microscopy. Its rice ortholog, OsABCG15 (also called Postmeiotic Deficient Anther 1, PDA1), is also required for exine development.21,22 pda1 displays aborted microspores without exine formation and vanished orbicules on tapetal cells. Because OsABCG15 protein is exclusively localized to the tapetal layer in a polar manner along the inner side of tapetal layer facing anther locule, it is thought to be mainly involved in the allocation of lipidic precursors for pollen exine formation.23 ABCG1 and ABCG16 are also required for pollen wall integrity, and atabcg1 atabcg16 double mutant has significantly reduced male fecundity, producing mainly collapsed pollens or pollens with defective nexine and intine. Therefore, ABCG1 and ABCG16 are involved in the transport of precursors for not only nexine but also intine formation. Owing to the lack of the phenotype of each individual single mutant,7 AtABCG1 and AtABCG16 jointly regulate pollen wall formation (Fig. 1). In addition, AtABCG9 and AtABCG31 are involved in the specific transport of steryl glycoside onto the surface of pollen for pollen tryphine deposition.12 atabcg9 atabcg31 displays collapsed or sticking pollens, resembling that of a steryl glycoside deficient mutant, ugt80A2 ugt80B1. Similarly, none of the individual single mutant shows visible phenotype. Notably, PpABCG7, a putative ortholog of AtABCG11 or AtABCG12 in the moss Physcomitrella patens, is required for the biosynthesis of the spore cuticle that is architecturally and compositionally comparable to those of flowering plants.25 These results indicate that ABCGs represent one of those genes that are conserved through plant evolution and required for the biosynthesis of the specialized cell wall, allowing the first terrestrial plants to survive in desiccating environments. Further investigations into the functional diversity across different
Gene expression pattern
Refs
unknown
25
AtABG11 is expressed in epidermal cells of both vegetative and reproductive organs. OsABCG26 is anther wall layers-specific expression. Tapetum-specific expression
8,9,23,28
Tapetum-specific expression
12
Tapetum and microsporesspecific expression
7
16-18,21,22
plant taxon will facilitate the understanding of the substrate specificity of those transporters. ABCG transporters and anther cuticle formation The male gametophyte is protected by another lipidic layer called anther cuticle, which shares common biosynthetic and transport genes with those of pollen exine.3,31 The anther wall contains 4 layers, namely the epidermis, the endothecium, the middle layer and the tapetal layer. Although it is known that an epidermis specific expressed gene, Wax deficient anther1 (Wda1), is involved in anther cuticle formation,2 increasing evidence shows that tapetum expressed genes contribute dominantly to the anther cuticle formation.3,31-33 In both cases, the transport of lipidic compounds across the plasma membrane of different layers of anther wall is indispensable. Compared with the transport of precursors from tapetel cell to anther locule for pollen wall formation, little is known about the transport of tapetel cell generated molecules to anther surface for anther cuticle formation until the recent identification of OsABCG26.23 The fact that OsABCG26 is localized in the epidermis, the endothecium and the tapetal layer at stage 9 (during which the middle layer becomes almost degenerated) and that numerous electron-dense lipidic granules inclusions are observed in osabcg26 along the tapetal cell locules wall adjacent to the middle layer provide the evidence that OsABCG26 is responsible for the transport of lipidic molecules from tapetum to anther wall layers for cuticle development. OsABCG15 is polarly localized in tapetal plasma membrane facing anther locules. This is different from that of OsABCG26. Because osabcg26osabcg15 double mutant mimics the phenotype of osabcg15 single mutant, it is plausible that OsABCG26 and OsABCG15 collaboratively regulate rice male reproduction.23 Interestingly, the Arabidopsis ortholog of OsABCG26, AtABCG11, is expressed in the embryo protoderm in a polar manner and in the endosperm, and is supposed to be involved in the formation of the endospermic cuticle in the boundaries between the endosperm and embryo or inner integumenta of
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Figure 1. Proposed model of ABCG transporters mediated allocation of tapetum generated anther cuticle and pollen wall components within anther tissues. In Arabidopsis, tapetal cells generated precursors for the formation of sexine, tryphine and nexine are transferred to anther locules by AtABCG26, AtABCG9 and AtABCG31, AtABCG1 and AtABCG16, crossing tapetal cells plasma membrane, which are then transferred to microspores surface by unknown transporters. AtABCG1 and AtABCG16 also export intine precursors across microspores plasma membrane for intine development. AtXs, unknown Arabidopisis ABCG transporters, are supposed to allocate cuticle precursor from tapetum to anther wall for cuticle formation. In rice, both OsABCG26 and OsABCG15 collaboratively regulate the transport of anther cuticle and sporopollenin precursors: while OsABCG26 mainly transport wax and cutin precursors toward anther surface for anther cuticle formation, OsABCG15 transport sporopollenin precursors from tapetum to anther locule for exine formation. OsC6, an lipid transport protein (LTP), also takes part in the transport of sporopollenin precursors in the anther locules for pollen exine formation. OsC6, on the other hand, may transfer lipidic precursors across cell spaces among different plasma membranes. Abbreviations: At26, AtABCG26; At9/31, AtABCG9 and AtABCG31; At1/16, AtABCG1 and AtABCG16; AtX, unknown Arabidopisis ABCG transporters; Ba, baculum; C, cuticle; Cp, cuticle precursors; E, epidermis; En, endothecium; In, intine; Ip, intine precursors; Lo, locules; Uts, unknown transporters; Ne, nexine; Np, nexine precursors; Os15, OsABCG15; Os26, OsABCG26; OsX, unknown rice ABCG importers; PM, plasma membrane; Sp, sporopollenin precursors; T, tapetum; Te, tectum; Ty, tryphine; Tp, tryphine precursors.
the seed coat.28 Clearly, functions of ABCGs also become divergent during the evolution.
involved in lipid transport.33 This suggests the existence of the conserved and diversified ABCG regulatory network at least in dicot and monocot plants.
The regulatory network of ABCG transporters Increasing evidence shows that there are conserved and divergent regulatory network governing lipid transport in plants, in which ABCG transporters are involved. Mutation of ABCGs often results in the reduction of the expression of many genes related to cutin or wax biosynthesis, modification and assembly. For example, mutation of AtABCG11 has a marked effect on the expression of cuticular lipid related genes in stems,28 among them are large CYP450s and GDSL-motif lipases. Mutation of OsABCG26 reduces remarkably the expression of several lipid biosynthetic and modifying genes including CYP704B2, CYP703A3, Defective Pollen Wall (DPW) and Wax-deficient anther1 (WDA1).23 Similar reduction of the expression of CYP704B2 and CYP703A3 is also observed in osabcg15 anthers.21 Therefore, the reduction of the anther cuticle and pollen wall precursors in these mutants results from direct reduction in transport and indirect reduction in biosynthesis. Upstream of this network, recent study reveals that ABORTED MICROSPORES (AMS), a master regulator of pollen wall development, directly regulates the expression of AtABCG26.34 Unfortunately, similar relationship between Tapetum Degeneration Retardation (TDR),33 the rice ortholog of AMS, and OsABCG15, the rice ortholog of AtABCG26, is not defined. However, TDR do directly regulate OsC6, another molecule
Perspectives and conclusions In flower plants, sperm cells are protected by 2 lipidic layers: the pollen wall and the anther cuticle. It is thought that the lipidic and phenolic components of the anther cuticle and pollen wall are synthesized in tapetum, while the components of intine are derived from microspores.35-39 Therefore, there are complex transport systems for the allocation of various structural constituents from tapetum to their destinations. ABCG transporters play critical roles in this process and mediates plant male reproductive development via regulating pollen wall development and anther cuticle formation. The half size ABCG transporters (WBC) require dimerization to form a functional ABCG transporter,6 which is also evidenced by the finding that AtABCG11 is capable of forming homodimer while ABCG12 is only capable of forming a dimer with ABCG11.40 However, whether other ABCG transporters form homo- or heter- dimmers to transport the precursors across anther wall layers remains unrevealed, particularly in rice and other crops. It is known that except ABCGs, many other transporters including lipid transport proteins are also involved in male reproduction via mediating the lipid allocation in reproductive organs.1,32,41 Unfortunately, the mechanisms
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underlying their modes of action and relationship with known ABCGs remain poorly understood. The chemical profiles of anther cuticle, pollen exine, and pollen tryphine vary significantly dependent mainly on species. Therefore, although ABCGs are conserved in plant taxon, different ABCGs may have or prefer to specific substrates restricted in certain species. The exact substrate of each ABCGs remains largely to be elucidated, and the substrate specificity may become more complicated because some ABCGs are promiscuous proteins with multiple partnerships. Given lipid molecule is hydrophobic, such a biochemical characterization is really a severe challenge. This mystery could be ultimately solved with the advance in biochemical and analytical methods and morphological characterization equipment. Tagged labeling combining with in situ imagining could also be an alternative. More and more evidence indicates that ABCGs work collaboratively to transport multiple precursors for cutin, wax, sporopollenin, tryphine, intine and nexine formation.7,12,23 Owing to the sharing of common aliphatic components between anther cuticle and pollen exine, some rice ABCGs transport similar or identical precursors for both anther cuticle and pollen wall formation, and this feature is not seen in Arabidopsis.1 Whether it is also true in Arabidopsis and other plant species merits further investigation. Closer investigation into the mutant phenotypes of rice ABCGs uncovers obvious alterations in the morphological structure of orbicules, the Ubish body,21,23,32,42 an unique ultrastructure that appears on the inner surface of the anther only in rice and other Poaceae plants but not in Arabidopsis and other Brassicaceae plants, which is supposed to transfer sporopollenin precursors from the tapetum to the pollen surface.37 This defective orbicules development is also seen in mutants of TDR, GAMYB and OsC6, both TDR and GAMYB are direct regulators of OsC6.33,43 Interestingly, this phenotype is seen as well in dpw,44 cyp704b2,3 cyp703a33.1 Therefore, orbicules may be the functional inner epidermal cuticle per se with similar chemical profiles to anther cuticle components and/or exine precursors. Thus, disruption of the functions of genes involved in either lipid biosynthesis (modification) or lipid transport affects the formation of orbicules and pollen wall as well. Nevertheless, the origin and the function of the orbicules in rice merits further clarification. In Arabidopsis, elaioplasts and tapetosomes are transporters for tryphine components.30 In summary, during the evolution, ABCGs emerge as one of the most conserved but also divergent proteins that safeguard the formation of male gametophyte via mediating the lipid metabolism, particularly the transport of the lipidic and phenolic precursors across both sides of anther layers to form the most important 2 protective barriers of pollen development. The in-depth functional characterization of these ABCGs will facilitate the elucidation of their molecular mechanisms on male reproduction.
Disclosure of potential conflicts of interest No potential conflicts of interest were disclosed.
Acknowledgments We would like to thank Dr. Frantisek Baluska for the invitation to write this review. This work was supported by funds from the National Natural Science Foundation of China (31230051, 30971739, 31270222, and 31110103915); China Innovative Research Team, Ministry of Education, and the Program of Introducing Talents of Discipline to Universities (111 Project, B14016); National Key Basic Research Developments Program, Ministry of Science and Technology, China (2013CB126902 and 2011CB100101); and a start-up grant to D.Z. from the School of Agriculture, Food and Wine, University of Adelaide.
Funding This work was supported by funds from the National Natural Science Foundation of China (31230051, 30971739, 31270222, and 31110103915); China Innovative Research Team, Ministry of Education, and the Program of Introducing Talents of Discipline to Universities (111 Project, B14016); National Key Basic Research Developments Program, Ministry of Science and Technology, China (2013CB126902 and 2011CB100101); and a startup grant to D.Z. from the School of Agriculture, Food and Wine, University of Adelaide.
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cuticular wax deposition and desiccation tolerance in the moss Physcomitrella patens. Plant Cell 2013; 25:4000-13; PMID:24163310; http://dx.doi.org/10.1105/tpc.113.117648 Landgraf R, Smolka U, Altmann S, Eschen-Lippold L, Senning M, Sonnewald S, Weigel B, Frolova N, Strehmel N, Hause G, et al. The ABC transporter ABCG1 is required for suberin formation in potato tuber periderm. Plant Cell 2014; 26(8):3403-15; PMID:25122151; http://dx.doi.org/10.1105/tpc.114.124776 Panikashvili D, Aharoni A. ABC-type transporters and cuticle assembly: linking function to polarity in epidermis cells. Plant Signal Behav 2008; 3:806-9; PMID:19704564; http://dx.doi.org/ 10.4161/psb.3.10.5887 Panikashvili D, Shi JX, Bocobza S, Franke RB, Schreiber L, Aharoni A. The Arabidopsis DSO/ABCG11 transporter affects cutin metabolism in reproductive organs and suberin in roots. Mol Plant 2010; 3:56375; PMID:20035035; http://dx.doi.org/10.1093/mp/ssp103 Fabre G, Garroum I, Mazurek S, Daraspe J, Mucciolo A, Sankar M, Humbel BM, Nawrath C. The ABCG transporter PEC1/ABCG32 is required for the formation of the developing leaf cuticle in Arabidopsis. New Phytologist 2015; 209(1):192-201; PMID:26406899 Quilichini TD, Samuels AL, Douglas CJ. ABCG26-mediated polyketide trafficking and hydroxycinnamoyl spermidines contribute to pollen wall exine formation in Arabidopsis. Plant Cell 2014; 26:4483-98; PMID:25415974; http://dx.doi.org/10.1105/ tpc.114.130484 Yang X, Wu D, Shi J, He Y, Pinot F, Grausem B, Yin C, Zhu L, Chen M, Luo Z, et al. Rice CYP703A3, a cytochrome P450 hydroxylase, is essential for development of anther cuticle and pollen exine. J Integr Plant Biol 2014; 56(10):979-94; PMID:24798002; http://dx.doi.org/ 10.1111/jipb.12212 Zhang D, Liang W, Yin C, Zong J, Gu F, Zhang D. OsC6, encoding a lipid transfer protein, is required for postmeiotic anther development in rice. Plant Physiol 2010; 154:149-62; PMID:20610705; http://dx.doi. org/10.1104/pp.110.158865 Li N, Zhang DS, Liu HS, Yin CS, Li XX, Liang WQ, Yuan Z, Xu B, Chu HW, Wang J, et al. The rice tapetum degeneration retardation gene is required for tapetum degradation and anther development. Plant Cell 2006; 18:2999-3014; PMID:17138695; http://dx.doi.org/10.1105/ tpc.106.044107 Xu J, Ding Z, Vizcay-Barrena G, Shi J, Liang W, Yuan Z, WerckReichhart D, Schreiber L, Wilson ZA, Zhang D. ABORTED MICROSPORES acts as a master regulator of pollen wall formation in Arabidopsis. Plant Cell 2014; 26:1544-56; PMID:24781116; http://dx.doi. org/10.1105/tpc.114.122986 Drakakaki G, Zabotina O, Delgado I, Robert S, Keegstra K, Raikhel N. Arabidopsis reversibly glycosylated polypeptides 1 and 2 are essential for pollen development. Plant Physiol 2006; 142:1480-92; PMID:17071651; http://dx.doi.org/10.1104/pp.106.086363 Huang L, Cao J, Zhang A, Ye Y, Zhang Y, Liu T. The polygalacturonase gene BcMF2 from Brassica campestris is associated with intine development. J Exp Bot 2009; 60:301-13; PMID:19039102; http://dx. doi.org/10.1093/jxb/ern295 Knox R, Heslop-Harrison J. Pollen-wall proteins: electron-microscopic localization of acid phosphatase in the intine of Crocus vernus. J Cell Sci 1971; 8:727-33; PMID:5087655 Moon S, Kim SR, Zhao GC, Yi J, Yoo Y, Jin P, Lee SW, Jung KH, Zhang D, An G. Rice GLYCOSYLTRANSFERASE1 encodes a glycosyltransferase essential for pollen wall formation. Plant Physiol 2013; 161:663-75; PMID:23263792; http://dx.doi.org/10.1104/pp.112.210948 Ueda K, Yoshimura F, Miyao A, Hirochika H, Nonomura K-I, Wabiko H. COLLAPSED ABNORMAL POLLEN1 gene encoding the arabinokinase-like protein is involved in pollen development in rice. Plant Physiol 2013; 162:858-71; PMID:23629836; http://dx.doi.org/ 10.1104/pp.113.216523 McFarlane HE, Shin JJH, Bird DA, Samuels AL. Arabidopsis ABCG transporters, which are required for export of diverse cuticular lipids, dimerize in different combinations. Plant Cell 2010; 22:3066-75; PMID:20870961; http://dx.doi.org/10.1105/tpc.110.077974 Huang M-D, Chen T-LL, Huang AH. Abundant type III lipid transfer proteins in Arabidopsis tapetum are secreted to the locule and become
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a constituent of the pollen exine. Plant Physiol 2013; 163:1218-29; PMID:24096413; http://dx.doi.org/10.1104/pp.113.225706 42. Huysmans S, El-Ghazaly G, Smets E. Orbicules in angiosperms: morphology, function, distribution, and relation with tapetum types. The Botanical Review 1998; 64:240-72; http://dx.doi.org/10.1007/BF02856566 43. Aya K, Ueguchi-Tanaka M, Kondo M, Hamada K, Yano K, Nishimura M, Matsuoka M. Gibberellin modulates anther development in rice via the transcriptional regulation of GAMYB.
Plant Cell 2009; 21:1453-72; PMID:19454733; http://dx.doi.org/ 10.1105/tpc.108.062935 44. Shi J, Tan H, Yu X-H, Liu Y, Liang W, Ranathunge K, Franke RB, Schreiber L, Wang Y, Kai G, et al. Defective pollen wall is required for anther and microspore development in rice and encodes a fatty acyl carrier protein reductase. Plant Cell 2011; 23:2225-46; PMID:21705642; http://dx.doi.org/10.1105/ tpc.111.087528
MINI-REVIEW
ATP binding cassette G transporters and plant male reproduction Guochao Zhaoa, Jianxin Shia, Wanqi Lianga, and Dabing Zhanga,b a
Joint International Research Laboratory of Metabolic & Developmental Sciences, Shanghai Jiao Tong University (SJTU)-University of Adelaide Joint Center for Agriculture and Health, State Key Laboratory of Hybrid Rice, School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai, China; bSchool of Agriculture, Food, and Wine, University of Adelaide, Urrbrae, South Australia, Australia
ABSTRACT
ARTICLE HISTORY
The function of ATP Binding Cassette G (ABCG) transporters in the regulation of plant vegetative organs development has been well characterized in various plant species. In contrast, their function in reproductive development particularly male reproductive development received considerably less attention till some ABCG transporters was reported to be associated with anther and pollen wall development in Arabidopsis thaliana and rice (Oryza sativa) during the past decade. This mini-review summarizes current knowledge of ABCG transporters regarding to their roles in male reproduction and underlying genetic and biochemical mechanisms, which makes it evident that ABCG transporters represent one of those conserved and divergent components closely related to male reproduction in plants. This mini-review also discusses the current challenges and future perspectives in this particular field.
Received 9 December 2015 Accepted 22 December 2015
Lipids and their derivatives, such as fatty acids and phospholipids are important structural components of the plant reproductive organs, therefore lipid metabolism plays important roles in plant reproduction.1 Similar to plant vegetative organs, the reproductive organ anther is also covered by a protective layer called cuticle, consisting mainly of lipid derived waxes and cutin components, which safeguards the normal development of the male gametophyte.2,3 The mature pollen has typical 3 wall structures (the outer exine, the inner intine, and the tryphine), which protects male gametophytes and facilitates male gamete survival and pollination (pistil-stigma interaction, pollen germination and hydration).1 The molecular mechanisms underlying the biosynthesis and modification of various lipidic precursors for anther cuticle and pollen wall formation in plant reproductive organs have been revealed via multiple approaches.1,4 Those studies highlight the coordinated function of sporophyte (tapetum) and gametocyte (pollen) in the process, and pinpoint the indispensable role of lipid transport in this process1,5 ATP Binding Cassette G (ABCG) transporters, comprising the half-size white/brown complex (WBC) transporters and the full-size pleiotropic drug resistance (PDR) subgroup members, are markedly expanded in plants, with more than 40 members in both Arabidopsis and rice.6 Although plant WBCs and PDRs are phylogenetically separated, both are associated with taxon-specific functional diversification, including plant defense and cuticle formation.6 In this mini-review, we focus mainly on those ABCG transporters in the context of their functions in male production, which is obviously functionally
CONTACT Dabing Zhang © 2016 Taylor & Francis Group, LLC
[email protected]
KEYWORDS
Anther cuticle; dimerization; male reproduction; pollen wall; sporopollenin
conserved at least between dicot Arabidopsis and monocot rice (Table 1). In past 2 decades, ABCG transporters in many plant species were identified to be involved in the cuticle secretion, transporting lipid molecules (precursors of wax, cutin and/or suberin) to across the plasma membrane to the epidermis. In Arabidopsis, the reported ones included AtABCG1, AtABCG2, AtABCG6, AtABCG16 and AtABCG20,7 AtABCG11,8,9 AtABCG12,10 AtABCG13,11 AtABCG9 and AtABCG31,12 AtABCG14,13-15 AtABCG26,16-18 AtABCG29,19 AtABCG32.20 In rice, the reported ABCG proteins were OsABCG15/ PDA1,21,22 OsABCG2623 and OsABCG31.24 Other reported ABCG proteins included Physco mitrella patens Pp-ABCG7,25 potato ABCG126 and barley HvABCG31.24 However, loss-offunction of some ABCG transporters affected profoundly plant development, particularly male reproductive organ development, leading to partial or complete sterile.11,16,21-23,27,28 It is worthy to note that most of the male reproduction associated ABCG transporters are half-size WBCs, although one full-size PDR, ABCG32/PEC1 (together with its ortholog in barley HvABCG31 and rice OsABCG31) also affects floral organ development.24,29
ABCG transporters and pollen wall development ABCG transporters play important roles in the allocation of various lipidic, phenolic, and other sporopollenin precursors and tryphine components from the tapetum where they are generated to the anther locule for pollen wall formation.1
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Table 1. ABCG transporters involved in the reproductive organs development. Gene name in Arabidopisis
Gene name in rice
Gene name in other species Pp-ABCG7
AtABG11
OsABCG26
AtABCG26
OsABCG15
AtABCG9 and AtABCG31 AtABCG1 and AtABCG16
Function Moss Physcomitrella patens Pp-ABCG7 affects spore wall architecture AtABG11 is involved in the formation of the cuticular barriers in both vegetative and reproductive organs. OsABCG26 is mainly responsible for the export of tapetum generated lipid precursors for anther cuticle formation. Both are involved in the transfer of sporopollenin precursors from tapetal cells to anther locules, facilitating exine formation These 2 genes collaboratively transfer tryphine components from tapetal cells to anther locules for tryphine deposition These 2 genes collaboratively transport nexine precursors from tapetal cells to anther locules and transport intine precursors across microspores plasma membrane for intine development
Arabidopsis AtABCG26 is responsible for the transport of polyketides for exine formation, and loss-of-function of ABCG26 results in significantly reduced fertility.16-18,30 atabcg26 mutant tapetal cells accumulate numerous electron-lucent vesicles and numerous electron-dense granules, and display accumulated large fluorescent vacuoles in tapetal cells with corresponding loss of fluorescence on microspores as evidenced by 2 photon microscopy. Its rice ortholog, OsABCG15 (also called Postmeiotic Deficient Anther 1, PDA1), is also required for exine development.21,22 pda1 displays aborted microspores without exine formation and vanished orbicules on tapetal cells. Because OsABCG15 protein is exclusively localized to the tapetal layer in a polar manner along the inner side of tapetal layer facing anther locule, it is thought to be mainly involved in the allocation of lipidic precursors for pollen exine formation.23 ABCG1 and ABCG16 are also required for pollen wall integrity, and atabcg1 atabcg16 double mutant has significantly reduced male fecundity, producing mainly collapsed pollens or pollens with defective nexine and intine. Therefore, ABCG1 and ABCG16 are involved in the transport of precursors for not only nexine but also intine formation. Owing to the lack of the phenotype of each individual single mutant,7 AtABCG1 and AtABCG16 jointly regulate pollen wall formation (Fig. 1). In addition, AtABCG9 and AtABCG31 are involved in the specific transport of steryl glycoside onto the surface of pollen for pollen tryphine deposition.12 atabcg9 atabcg31 displays collapsed or sticking pollens, resembling that of a steryl glycoside deficient mutant, ugt80A2 ugt80B1. Similarly, none of the individual single mutant shows visible phenotype. Notably, PpABCG7, a putative ortholog of AtABCG11 or AtABCG12 in the moss Physcomitrella patens, is required for the biosynthesis of the spore cuticle that is architecturally and compositionally comparable to those of flowering plants.25 These results indicate that ABCGs represent one of those genes that are conserved through plant evolution and required for the biosynthesis of the specialized cell wall, allowing the first terrestrial plants to survive in desiccating environments. Further investigations into the functional diversity across different
Gene expression pattern
Refs
unknown
25
AtABG11 is expressed in epidermal cells of both vegetative and reproductive organs. OsABCG26 is anther wall layers-specific expression. Tapetum-specific expression
8,9,23,28
Tapetum-specific expression
12
Tapetum and microsporesspecific expression
7
16-18,21,22
plant taxon will facilitate the understanding of the substrate specificity of those transporters. ABCG transporters and anther cuticle formation The male gametophyte is protected by another lipidic layer called anther cuticle, which shares common biosynthetic and transport genes with those of pollen exine.3,31 The anther wall contains 4 layers, namely the epidermis, the endothecium, the middle layer and the tapetal layer. Although it is known that an epidermis specific expressed gene, Wax deficient anther1 (Wda1), is involved in anther cuticle formation,2 increasing evidence shows that tapetum expressed genes contribute dominantly to the anther cuticle formation.3,31-33 In both cases, the transport of lipidic compounds across the plasma membrane of different layers of anther wall is indispensable. Compared with the transport of precursors from tapetel cell to anther locule for pollen wall formation, little is known about the transport of tapetel cell generated molecules to anther surface for anther cuticle formation until the recent identification of OsABCG26.23 The fact that OsABCG26 is localized in the epidermis, the endothecium and the tapetal layer at stage 9 (during which the middle layer becomes almost degenerated) and that numerous electron-dense lipidic granules inclusions are observed in osabcg26 along the tapetal cell locules wall adjacent to the middle layer provide the evidence that OsABCG26 is responsible for the transport of lipidic molecules from tapetum to anther wall layers for cuticle development. OsABCG15 is polarly localized in tapetal plasma membrane facing anther locules. This is different from that of OsABCG26. Because osabcg26osabcg15 double mutant mimics the phenotype of osabcg15 single mutant, it is plausible that OsABCG26 and OsABCG15 collaboratively regulate rice male reproduction.23 Interestingly, the Arabidopsis ortholog of OsABCG26, AtABCG11, is expressed in the embryo protoderm in a polar manner and in the endosperm, and is supposed to be involved in the formation of the endospermic cuticle in the boundaries between the endosperm and embryo or inner integumenta of
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Figure 1. Proposed model of ABCG transporters mediated allocation of tapetum generated anther cuticle and pollen wall components within anther tissues. In Arabidopsis, tapetal cells generated precursors for the formation of sexine, tryphine and nexine are transferred to anther locules by AtABCG26, AtABCG9 and AtABCG31, AtABCG1 and AtABCG16, crossing tapetal cells plasma membrane, which are then transferred to microspores surface by unknown transporters. AtABCG1 and AtABCG16 also export intine precursors across microspores plasma membrane for intine development. AtXs, unknown Arabidopisis ABCG transporters, are supposed to allocate cuticle precursor from tapetum to anther wall for cuticle formation. In rice, both OsABCG26 and OsABCG15 collaboratively regulate the transport of anther cuticle and sporopollenin precursors: while OsABCG26 mainly transport wax and cutin precursors toward anther surface for anther cuticle formation, OsABCG15 transport sporopollenin precursors from tapetum to anther locule for exine formation. OsC6, an lipid transport protein (LTP), also takes part in the transport of sporopollenin precursors in the anther locules for pollen exine formation. OsC6, on the other hand, may transfer lipidic precursors across cell spaces among different plasma membranes. Abbreviations: At26, AtABCG26; At9/31, AtABCG9 and AtABCG31; At1/16, AtABCG1 and AtABCG16; AtX, unknown Arabidopisis ABCG transporters; Ba, baculum; C, cuticle; Cp, cuticle precursors; E, epidermis; En, endothecium; In, intine; Ip, intine precursors; Lo, locules; Uts, unknown transporters; Ne, nexine; Np, nexine precursors; Os15, OsABCG15; Os26, OsABCG26; OsX, unknown rice ABCG importers; PM, plasma membrane; Sp, sporopollenin precursors; T, tapetum; Te, tectum; Ty, tryphine; Tp, tryphine precursors.
the seed coat.28 Clearly, functions of ABCGs also become divergent during the evolution.
involved in lipid transport.33 This suggests the existence of the conserved and diversified ABCG regulatory network at least in dicot and monocot plants.
The regulatory network of ABCG transporters Increasing evidence shows that there are conserved and divergent regulatory network governing lipid transport in plants, in which ABCG transporters are involved. Mutation of ABCGs often results in the reduction of the expression of many genes related to cutin or wax biosynthesis, modification and assembly. For example, mutation of AtABCG11 has a marked effect on the expression of cuticular lipid related genes in stems,28 among them are large CYP450s and GDSL-motif lipases. Mutation of OsABCG26 reduces remarkably the expression of several lipid biosynthetic and modifying genes including CYP704B2, CYP703A3, Defective Pollen Wall (DPW) and Wax-deficient anther1 (WDA1).23 Similar reduction of the expression of CYP704B2 and CYP703A3 is also observed in osabcg15 anthers.21 Therefore, the reduction of the anther cuticle and pollen wall precursors in these mutants results from direct reduction in transport and indirect reduction in biosynthesis. Upstream of this network, recent study reveals that ABORTED MICROSPORES (AMS), a master regulator of pollen wall development, directly regulates the expression of AtABCG26.34 Unfortunately, similar relationship between Tapetum Degeneration Retardation (TDR),33 the rice ortholog of AMS, and OsABCG15, the rice ortholog of AtABCG26, is not defined. However, TDR do directly regulate OsC6, another molecule
Perspectives and conclusions In flower plants, sperm cells are protected by 2 lipidic layers: the pollen wall and the anther cuticle. It is thought that the lipidic and phenolic components of the anther cuticle and pollen wall are synthesized in tapetum, while the components of intine are derived from microspores.35-39 Therefore, there are complex transport systems for the allocation of various structural constituents from tapetum to their destinations. ABCG transporters play critical roles in this process and mediates plant male reproductive development via regulating pollen wall development and anther cuticle formation. The half size ABCG transporters (WBC) require dimerization to form a functional ABCG transporter,6 which is also evidenced by the finding that AtABCG11 is capable of forming homodimer while ABCG12 is only capable of forming a dimer with ABCG11.40 However, whether other ABCG transporters form homo- or heter- dimmers to transport the precursors across anther wall layers remains unrevealed, particularly in rice and other crops. It is known that except ABCGs, many other transporters including lipid transport proteins are also involved in male reproduction via mediating the lipid allocation in reproductive organs.1,32,41 Unfortunately, the mechanisms
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underlying their modes of action and relationship with known ABCGs remain poorly understood. The chemical profiles of anther cuticle, pollen exine, and pollen tryphine vary significantly dependent mainly on species. Therefore, although ABCGs are conserved in plant taxon, different ABCGs may have or prefer to specific substrates restricted in certain species. The exact substrate of each ABCGs remains largely to be elucidated, and the substrate specificity may become more complicated because some ABCGs are promiscuous proteins with multiple partnerships. Given lipid molecule is hydrophobic, such a biochemical characterization is really a severe challenge. This mystery could be ultimately solved with the advance in biochemical and analytical methods and morphological characterization equipment. Tagged labeling combining with in situ imagining could also be an alternative. More and more evidence indicates that ABCGs work collaboratively to transport multiple precursors for cutin, wax, sporopollenin, tryphine, intine and nexine formation.7,12,23 Owing to the sharing of common aliphatic components between anther cuticle and pollen exine, some rice ABCGs transport similar or identical precursors for both anther cuticle and pollen wall formation, and this feature is not seen in Arabidopsis.1 Whether it is also true in Arabidopsis and other plant species merits further investigation. Closer investigation into the mutant phenotypes of rice ABCGs uncovers obvious alterations in the morphological structure of orbicules, the Ubish body,21,23,32,42 an unique ultrastructure that appears on the inner surface of the anther only in rice and other Poaceae plants but not in Arabidopsis and other Brassicaceae plants, which is supposed to transfer sporopollenin precursors from the tapetum to the pollen surface.37 This defective orbicules development is also seen in mutants of TDR, GAMYB and OsC6, both TDR and GAMYB are direct regulators of OsC6.33,43 Interestingly, this phenotype is seen as well in dpw,44 cyp704b2,3 cyp703a33.1 Therefore, orbicules may be the functional inner epidermal cuticle per se with similar chemical profiles to anther cuticle components and/or exine precursors. Thus, disruption of the functions of genes involved in either lipid biosynthesis (modification) or lipid transport affects the formation of orbicules and pollen wall as well. Nevertheless, the origin and the function of the orbicules in rice merits further clarification. In Arabidopsis, elaioplasts and tapetosomes are transporters for tryphine components.30 In summary, during the evolution, ABCGs emerge as one of the most conserved but also divergent proteins that safeguard the formation of male gametophyte via mediating the lipid metabolism, particularly the transport of the lipidic and phenolic precursors across both sides of anther layers to form the most important 2 protective barriers of pollen development. The in-depth functional characterization of these ABCGs will facilitate the elucidation of their molecular mechanisms on male reproduction.
Disclosure of potential conflicts of interest No potential conflicts of interest were disclosed.
Acknowledgments We would like to thank Dr. Frantisek Baluska for the invitation to write this review. This work was supported by funds from the National Natural Science Foundation of China (31230051, 30971739, 31270222, and 31110103915); China Innovative Research Team, Ministry of Education, and the Program of Introducing Talents of Discipline to Universities (111 Project, B14016); National Key Basic Research Developments Program, Ministry of Science and Technology, China (2013CB126902 and 2011CB100101); and a start-up grant to D.Z. from the School of Agriculture, Food and Wine, University of Adelaide.
Funding This work was supported by funds from the National Natural Science Foundation of China (31230051, 30971739, 31270222, and 31110103915); China Innovative Research Team, Ministry of Education, and the Program of Introducing Talents of Discipline to Universities (111 Project, B14016); National Key Basic Research Developments Program, Ministry of Science and Technology, China (2013CB126902 and 2011CB100101); and a startup grant to D.Z. from the School of Agriculture, Food and Wine, University of Adelaide.
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