Computational Biology and Chemistry 51 (2014) 63–70

Contents lists available at ScienceDirect

Computational Biology and Chemistry journal homepage: www.elsevier.com/locate/compbiolchem

Structure and evolution analysis of pollen receptor-like kinase in Zea mays and Arabidopsis thaliana Dongxu Wang 1, He Wang 1, Muhammad Irfan, Mingxia Fan **, Feng Lin * Biotechnology and Bioscience College, Shenyang Agricultural University, 120 Dongling Road, Shenyang, Liaoning 110866, China

A R T I C L E I N F O

A B S T R A C T

Article history: Received 7 May 2014 Received in revised form 2 June 2014 Accepted 23 June 2014 Available online 25 June 2014

Receptor-like kinase (RLKs) is an important member in protein kinase family which is widely involved in plant growth, development and defense responses. It is significant to analyze the kinase structure and evolution of pollen RLKs in order to study their mechanisms. In our study, 64 and 73 putative pollen RLKs were chosen from maize and Arabidopsis. Phylogenetic analysis showed that the pollen RLKs were conservative and might had existed before divergence between monocot and dicot which were mainly concentrated in RLCK-VII and LRR-III two subfamilies. Chromosomal localization and gene duplication analysis showed the expansion of pollen RLKs were mainly caused by segmental duplication. By calculating Ka/Ks value of extracellular domain, intracellular domain and kinase domain in pollen RLKs, we found that the pollen RLKs duplicated genes had mainly experienced the purifying selection, while maize might have experienced weaker purifying selection. Meanwhile, extracellular domain might have experienced stronger diversifying selection than intracellular domain in both species. Estimation of duplication time showed that the duplication events of Arabidopsis have occurred approximately between 18 and 69 million years ago, compared to 0.67–170 million years ago of maize. ã 2014 Elsevier Ltd. All rights reserved.

Keywords: Pollen RLKs Phylogenetic evolution Gene duplication

1. Introduction During the double fertilization process in plants, a series of activities of pollen tube are controlled by male and female tissues from stigma to female gametophyte with regulation of many proteins and signaling molecules (Chen et al., 2014; Higashiyama and Hamamura, 2008; Beale and Johnson, 2013). Receptor-like kinase (RLKs) as a big subfamily in protein kinase widely participate in various signal transduction processes, its two main functions include controlling plant growth and development; involving in plant–microbe interactions and defense responses (Shiu and Bleecker, 2001). Most RLKs consisting of a ligandidentifying and signal-accepting extracellular domain, a transmembrane domain, and an intracellular domain with kinase activity (Stone and Walker, 1995). RLKs have received the widespread attention since the first receptor-like kinase was found in maize over 20 years ago (Walker and Zhang, 1990).

* Corresponding author. Tel.: +86 13840386419. ** Corresponding author. E-mail addresses: [email protected] (M. Fan), [email protected] (F. Lin). 1 These authors have equal contribution to the paper. http://dx.doi.org/10.1016/j.compbiolchem.2014.06.001 1476-9271/ ã 2014 Elsevier Ltd. All rights reserved.

Subsequently, many RLKs members have been identified in other plant species (Shiu et al., 2004). Currently, many experiments showed that RLKs can be involved directly in pollen development, pollen and stigma interactions, pollen tube growth and interaction with the guidance tissues, pollen tube and ovule interactions, as well as the pollen tube rupture in the embryo sac. For example, one lectin receptor-like kinase SGC in Arabidopsis can influence the normal development of pollen (Wan et al., 2008). PiPRK1 in Petunia inflata can specifically expressed in pollen and pollen tubes, the antisense gene could cause half transgenic pollen sterility (Mu et al.,1994; Lee et al.,1996). The pistil determinant SRK in Brassica can participate in pollen selfincompatibility (Takasaki et al., 2000; Stein et al., 1991). RKF1 expressed in Arabidopsis stamen may play a critical role in microsporogenesis, pollen maturation, or pollen–stigma interactions (Takahashi et al., 1998). AtPRK1 and AtPRK2 in Arabidopsis and LePRK1, LePRK2, LePRK3 in tomato can control pollen germination and elongation (Zhang and McCormick, 2007; Muschietti et al., 1998; Tang et al., 2002, 2004). AtPRK1 and AtPRK2 activate RopGEF1 by phosphorylation, thereby control the polar growth of pollen tube (Chang et al., 2013). While LePRK2 maybe influence the normal function of the pollen tube by regulating actin distribution (Salem et al., 2011; Xu and Huang, 2014). In addition, certain receptor-like kinase can regulate the pollen development indirectly. For example, the leucine-rich repeat

64

D. Wang et al. / Computational Biology and Chemistry 51 (2014) 63–70

receptor-like kinases (LRR-RLKs) BAM1/BAM2 (DeYoung et al., 2006; Hord et al., 2006), EMS1/EXS (Canales et al., 2002; Zhao et al., 2002), MSP1 (Nonomura et al., 2003), SERK1/SERK2 (Albrecht et al., 2005; Colcombet et al., 2005), GhSERK (Shi et al., 2014), ER family (ER, ERL1 ERL2) (Hord et al., 2008) as well as RPK2 (Mizuno et al., 2007) play role in early anther cell differentiation process. These RLKs influence pollen development indirectly by controlling tapetum development. While, the function of some pollen RLKs has not been studied in depth, their roles in pollen development and related activities remain to be discovered. Such as pollen specific receptor-like kinase ZmPRK1 in maize, AtPRK3 and AtPRKb in Arabidopsis and others (Kim et al., 2002). From above examples, we can know that the function of RLKs is closely related to its own structure, after the signal molecule identified by extracellular N-terminal signal peptide and bind with receptor domain. It can be transmitted into intracellular through transmembrane domains, and received by intracellular kinase domain. This open or close the downstream target proteins through phosphorylation or dephosphorylation, to start a signal cascade reaction (Malho et al., 2006). RLKs are composed of a complex signal path with upstream and downstream component, and regulate the signal response of plant by transmitting signal through phosphorylation (Antolín-Llovera et al., 2012; Dai et al., 2013). With this kind of mechanism, pollen receptor-like kinase are extensively involved in the double fertilization process. The similarity and difference of its function, as well as the location and time of working, suggesting that each sequence must have their own characteristics on the basic of similarity. In this paper, we use the phylogenetic analysis of pollen receptor-like kinase to briefly analyze the relationship between its kinase domain structure and classification of pollen RLKs; and analyze their differences and correlations in evolutionary terms by comparative studying pollen receptor-like kinases in the dicot Arabidopsis and monocot maize. 2. Materials and methods 2.1. Search of pollen receptor-like kinase In this study, nearly 20 years of published articles reporting pollen receptor-like kinases which can be directly involved in the process from pollen development to pollen fertilization were searched and used as base material. The BLASTp in GRAMENE (http://www.gramene.org/) and TAIR (http://www.arabidopsis. org/) was used to search for homologues sequence of pollen receptor-like kinase. After that three database websites genevestigator, AtGenExpress Visualization Tool and MaizeGDB were used to predict the expression of these candidate sequences. Finally, we choose the ones that have higher expression level in Arabidopsis and maize pollen as a follow-up research target. 2.2. Phylogenetic and structure analysis of kinase Twenty pollen RLKs searched from articles and all putative maize and Arabidopsis pollen RLKs predicted were aligned using

ClustalX v1.83, respectively, Phylogenetic tree was constructed using MEGA 5.0 by neighbor-joining (NJ) method. Bootstrap values have been calculated from 1000 iterations. Other parameters were set as the system default value. The kinases active-sites of known pollen RLKs were predicted by ScanProsite (http://prosite.expasy. org/scanprosite/) and the structures of RLKs were predicted by SMART (http://smart.embl-heidelberg.de/). 2.3. Chromosomal locations of pollen RLKs in Zea mays and Arabidopsis Zea mays and Arabidopsis pollen RLKs were performed on chromosomes according to their staring positions given in the GRAMENE (http://www.maizegenome.org/data_portal.html) and TAIR (http://www.arabidopsis.org/) databases. MapInspect software (http://www.plantbreeding.wur.nl/uk/software_mapinspect. html) was subsequently used for generating image of all Zea mays and Arabidopsis putative pollen RLKs gene location. 2.4. Pollen RLKs gene duplication in Zea mays and Arabidopsis To analyze the gene duplication events, the multiple sequence alignment of the Zea mays and Arabidopsis putative pollen RLKs gene was performed by ClustalW and calculated using MEGA v5.0, respectively. Then, the gene pairs whose bootstrap value >99 were chosen, and were put on the chromosomes map. 2.5. Estimation of substitution rate and duplication time The nonsynonymous substitution rate (Ka) and the synonymous substitution rate (Ks) were calculated for ECDs, ICDs, and kinase domains using the DnaSPv5.0 software. The ratio of nonsynonymous to synonymous nucleotide substitutions (Ka/Ks) between paralogs was analyzed to detect the mode of selection. For inferring the dates of gene duplications, only the kinase domain coding sequences were used. The Ks value was translated into duplication time in million years based on a rate of l substitutions per synonymous site per year (Peng et al., 2012). The duplication time (T) was calculated as T = Ks/2l  10 6 Mya (Lynch and Conery, 2000) (l = 6.5  10 9 for maize and l = 1.5  10 8 for Arabidopsis) (Blanc and Wolfe, 2004; Yu et al., 2005). 3. Results and discussion The function of RLKs depend on ligands. However, most ligands of RLKs have not been found yet. By comparison, the ligands of LePRK1 and LePRK2 in tomato have been made comparatively deep research (Table 1). Depending on the perception and transduction of RLKs, the ligands were involved in germination and elongation of tomato pollen tube (Tang et al., 2002; Salem et al., 2012). At the same time, both male and female ligands were needed in participating in a series of physiological processes in pollen (Fig. 1).

Table 1 The ligands of LePRKs in tomato. Ligand

Source Binding site

Function

LAT52

Pollen

LeSHY

Pollen

Pollen hydration and pollen tube growth Muschietti et al. (1994), Wengier et al. (2003), Tang et al. (2002) Pollen germination and pollen tube Tang et al. (2004) growth Guyon et al. (2004) Pollen tube growth Tang et al. (2004)

LeSTIG1 STIL KPP

Extracellular domain of LePRK2

Extracellular domain of LePRK1 and LePRK2 Stigma Extracellular domain of LePRK1 and LePRK2 Style LePRK complexes Pollen Intracellular domain of LePRK1 and LePRK2

Pollen tube growth Polarity growth of pollen tube

References

Wengier et al. (2010) Kaothien et al. (2005)

D. Wang et al. / Computational Biology and Chemistry 51 (2014) 63–70

65

Fig. 1. Interactions of ligands and LePRKs before and after pollen germination. Numerous ligands (solid line represents the ligands generated from pollen; dotted line represents the ligands generated from pistil) interact with the extracellular domain of LePRKs, the signal transmit downstream via the transmembrane domain. PM represents plasma membrane; JM (Juxtamembrane) is the region which closely related to the interaction of LePRK1 and LePRK2.

3.1. Search of pollen receptor-like kinase In this study, 20 known pollen receptor like kinases (RLKs) which directly related to pollen were searched from previously published articles. These pollen RLKs were FERONIA (AEE78805), ANXUR1 (AEE74120), ANXUR2 (AED93826), LIP1 (AED92301), LIP2 (AAE73862), AtPRK1 (AAC13607), AtPRK2 (AEC06031), SGC (AEE79146), AtPRK3 (CAB86675), AtPRKb (AC012561) RKF1 (AEE31125), AtSRK (AGC55015) from Arabidopsis; PiPRK1 (AAA33715) from Petunia inflate ; LePRK1 (AAC12254), LePRK2 (AAC11253), LePRK3 (AF243040) from tomato; SRK (Q09092) from Brassica and ZmUPRK1 (AAK73111), ZmUPRK2 (AFW64201), ZmPRK1 (AAK28346) from maize. 3.2. Chromosomal locations and gene duplication of pollen RLKs in maize and Arabidopsis These 20 reported pollen RLKs were used as BLASTp queries, the expression of all obtained sequences were predicted by three databases (genevestigator; AtGenExpress Visualization Tool and MaizeGDB). Finally, we got 64 putative pollen RLKs gene in maize and 73 putative pollen RLKs gene in Arabidopsis which can express at a higher level in pollen tissues. Then the staring positions on chromosomes of these genes were given in GRAMENE (http:// www.maizegenome.org/data_portal.html) and TAIR (http://www. arabidopsis.org/) databases, the results shown in Fig. 2. Gene duplication is the main reason for evolution (Sankoff, 2001). After experienced several genome duplication event, the diversity of each species become richer. Based on the starting position of each gene on the chromosomes, the 64 maize putative pollen RLKs genes were found to be randomly distributed on chromosomes 1–10 (Fig. 2A). But the distribution was uneven, chromosome 5 and chromosome 10 contained the least number of maize pollen RLKs genes, both of them contained only 2 genes, while the number of genes on other chromosomes was more evenly distributed. Similarly, the 73 Arabidopsis pollen RLKs genes also showed uneven density distribution, and most of them were located at the beginning and the endings of chromosomes (Fig. 2B). The AtSRK was not mapped on any chromosome due to lack of information. Holub (2001) defined the gene cluster as a chromosome region which contains two or more genes within 200 KB. In our study, clusters can be found both in maize and Arabidopsis, while clusters in Arabidopsis are quite obvious, 22 genes were located in 10 clusters on the 5 chromosomes. By contrast, only 3 clusters were

present on maize chromosome 4. On the other hand, based on the phylogenetic analysis and the chromosomal locations of the pollen RLKs genes, 12 segmental duplication events (24 genes) and 11 segmental duplication events (22 genes) were found located in pollen RLKs genes in maize and Arabidopsis, respectively (Fig. 2). These segmental duplication events occurred on all chromosomes in these two species except chromosomes 10 in maize. The pollen RLKs might exist before divergence between monocot and dicot. The number of pollen RLKs in maize were not match its huge genome number, which might be due to the gene chip technology in maize which was not perfect or gene conservative and slow during evolutionary process. Gene duplication which can be divided into tandem and segmental duplications is one of the common mechanisms throughout the evolutionary process of genomes (Leister, 2004). According to the physical map location of the pollen RLKs, 12 and 11 gene pairs from maize and Arabidopsis involved gene duplication were identified, and all of them belongs to segmental duplications, indicating that segmental duplications seems to be the main mechanism in promoting pollen RLKs family lineage expansion. 3.3. Phylogenetic and structural analysis of known pollen RLKs A neighbor-joining (NJ) tree was constructed based on the alignment of the kinase sequences of the 20 pollen RLKs (Fig. 3A). It was found that some sequences which have similar functions were not clustered strictly together like, PiPRK, ZmUPRK1 and ZmUPRK2. It was suggested that the function of PiPRK may not be single during pollen development. In addition to regulating pollen development, PiPRK might also play role in pollen germination and elongation. While ZmUPRK1 and ZmUPRK2 might have different mechanisms from other RLKs in promoting pollen tube elongation. RKF1 and SRK which belongs to different subfamilies were clustered together, indicating that they might have similarities in function. It was worth noting that the phylogenetic tree also showed obvious kinship and this kind of classification was closely related to the kinase active-site. The sequences whose active-site was Asp were clustered, and ones whose active-site was Asn and His were clustered (Fig. 3B). The structures of kinase domain were predicted by SMART (Fig. 3C), and many RLKs subfamilies were involved in pollen development. The RLKs which contain extracellular domain, a transmembrane domain and intracellular domain and the ones which contain only intracellular domain (cytoplasmic kinase, RLCK) were included. It

66

D. Wang et al. / Computational Biology and Chemistry 51 (2014) 63–70

Fig. 2. Physical locations of the pollen RLKs genes on the Zea mays (A) and Arabidopsis (B). The chromosome numbers are indicated at the top of each chromosome and the left side of each chromosome is related to the approximate physical location of each pollen RLKs gene. The segmental duplication genes are connected by thin black lines, and the gene clusters are marked by red lines.

reflects that it was feasible to search nearly all pollen RLKs using these 20 pollen RLKs. The clustering results were consistent with kinase active-sites, indicating that the active site of the kinase plays an important role during functioning. LePRK3 might had different function with LePRK1 and LePRK2, though they were in the same family (Kim et al., 2002), this conclusion was consistent with our findings (Fig. 2B). Meanwhile, RKF1 and SRK which belong to different subfamilies were clustered together, indicating that maybe they

have same functions which confirms the prediction of Takahashi et al. (1998) that RKF1 might be involved in stigma-pollen recognition. 3.4. Phylogenetic analysis of pollen RLKs in Zea mays and Arabidopsis In order to understand the differences and similarities about evolutionary relationships between monocots (Zea mays) and dicots (Arabidopsis), the kinase domains were used to align for

D. Wang et al. / Computational Biology and Chemistry 51 (2014) 63–70

67

Fig. 3. The kinase domain phylogeny and domain configurations of known pollen RLKs. (A) Kinase phylogenetic tree of known pollen RLKs. The phylogeny was generated using kinase domain amino acid sequences of 20 pollen RLKs chosen from articles. The subfamily designations are based on a published classification scheme (Shiu and Bleecker, 2003). (B) Prediction of kinase active-site. (C) Representative domain organizations for known pollen RLKs subfamilies. The pollen RLKs subfamilies are divided into receptor-like kinase (RLK) and cytoplasmic kinase (RLCK), and the domains of pollen RLKs is predicted by SMART.

constructing phylogenetic tree (Fig. 4). According to the phylogenetic analysis, pollen RLKs were divided into 8 groups which including 18 subfamilies. Among them, RLCK-VII and LRR-III include the largest gene numbers. Meanwhile, maize (blue line) and

Arabidopsis (pink line) were not clustered separately, indicating that pollen RLKs in maize and Arabidopsis was quite conservative, probably came from the same ancestor. This indicated that pollen RLKs existed before divergence between monocot and dicot.

Fig. 4. The kinase domain phylogeny of putative pollen RLKs members from Zea mays and Arabidopsis. The phylogeny was generated using kinase domain amino acid sequences of putative pollen RLKs from Arabidopsis and Zea mays, which were color-coded blue and pink, respectively. The 8 group were emphasized by different colors (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

68

D. Wang et al. / Computational Biology and Chemistry 51 (2014) 63–70

3.5. Substitution rate and duplication time estimates for pollen RLK domains To investigate and comparatively analyze the differences in selective constraints, the best matches of pollen RLKs from both maize and Arabidopsis were identified. An alignment was generated for each pair. The synonymous and nonsynonymous substitution rates (Ka and Ks) for the extracellular domains (ECD), intracellular domains (ICD), and kinase domains of each pair from maize and Arabidopsis were calculated. The kinase domain sequences were used to estimate duplication time. Generally, the ratio of Ka/Ks > 1 indicates accelerated evolution with positive selection, the ratio = 1 indicates neutral selection, while the ratio < 1 indicates negative or purifying selection (Juretic et al., 2005). In this study, the majority of gene pairs in three domains from maize and Arabidopsis were under purifying selection, and the Ka/Ks ratios for most of them being even less than 0.4, suggesting strong purifying selection (Fig. 5A). Only three duplicated pairs seem to be under positive selection. All of these results suggested that

functions of the pollen RLKs genes did not diverge much along with the genome evolution after the duplication events. The Ka/Ks ratios of ICD, ECD and kinase domain from maize and Arabidopsis were calculated in order to understand the different evolution characteristics. The Ka/Ks ratios of maize genes were higher than Arabidopsis genes in all these three domains, indicating that the purifying selection of maize was more moderate (Fig. 5). Interestingly, the frequency distribution of ECDs was significantly different from those of ICDs and kinase domains, and the Ka/Ks ratios of ECDs was the highest. This result was in accordance with findings of Shiu et al. (2004). That means the ECDs evolved faster during evolution or relaxed purifying selection. Compared with ICDs, the duplicated pairs with Ka/Ks ratio > 1 were generally in the ECDs, indicating that parts of the extracellular regions of some pollen RLKs might have experienced positive selection. The kinase domains were used to estimate the duplication time, the Ks value of each gene pairs were used to calculate the duplication dates. The duplication events of Arabidopsis have occurred approximately between 18 and 69 million years ago

Fig. 5. The Ka/Ks ratios for different domains in pollen RLKs in maize and Arabidopsis. (A) The overall trend of Ka/Ks ratios for ECDs, ICDs and kinase domain in pollen RLKs of maize and Arabidopsis. Blue regions represents the Ka/Ks ratios < 0.4. The line indicates a one-to-one relationship between Ka and Ks. (B)–(D) The Ka/Ks frequency distribution for ECD, ICD, and kinase, respectively. The average Ka/Ks for each domain is indicated by an arrowhead (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

D. Wang et al. / Computational Biology and Chemistry 51 (2014) 63–70

(Mya), while the span for duplication time of maize was quite large, between 0.67 and 170 million years ago. Evolutionary analysis about ICDs, ECDs, and kinase domain of pollen RLKs showed that the Ka/Ks ratio of monocot maize was higher than dicots Arabidopsis, indicating that maize might have experienced weaker purifying selection. Whether in maize or Arabidopsis, Ka/Ks values of extracellular domain were higher than intracellular domain. It also highlights the possibility that only certain residues of the ECDs were under positive selection, these findings were consistent with the point that the ECDs of pollen RLKs might have experienced stronger diversifying selection for recognizing various extracellular signals. By contrast, the ICDs might have been under stronger purifying selection because of functional constraints in transducing signals to downstream components faithfully (Shiu et al., 2004). Estimation of duplication time in maize and Arabidopsis pollen RLKs showed that the duplication of maize genome was more distant, indicating that some genes duplication may occurred before divergence between monocot and dicot (Sanderson, 1997; Chaw et al., 2004). These genes were preserved and duplication events still occur after the separation between monocot and dicot. The function of several members of the pollen RLKs have been studied deeply, while the majority of pollen RLKs still remain to study further. 4. Conclusion In conclusion, all of these pollen RLKs can be divided into 8 subfamilies, and mainly concentrated in RLCK-VII and LRR-III two subfamilies in monocots and dicots. Further analysis showed that monocots have weaker selection as compared to dicots. Segmental duplications are the main causes of expansion of pollen RLKs. The event duplication time was also studied which showed evolutionary history of these RLKs. The results of this study are very helpful in studying further molecular evolution and detailed mechanism of RLKs. References Albrecht, C., Russinova, E., Hecht, V., Baaijens, E., de Vries, S., 2005. The Arabidopsis thaliana somatic embryogenesis receptor-like kinases 1 and 2 control male sporogenesis. Plant Cell 17, 3337–3349. Antolín-Llovera, N., Ried, M.K., Binder, A., Parniske, M., 2012. Receptor kinase signaling pathways in plant–microbe interactions. Ann. Rev Phytopathol. 50, 451–473. Beale, K.M., Johnson, M.A., 2013. Speed dating, rejection, and finding the perfect mate: advice from flowering plants. Curr. Opin. Plant Biol. 16, 590–597. Blanc, G., Wolfe, K.H., 2004. Widespread paleopolyploidy in model plant species inferred from age distributions of duplicate genes. Plant Cell 16, 1667–1678. Canales, C., Bhatt, A.M., Scott, R., Dickinson, H., 2002. EXS, a putative LRR receptor kinase, regulates male germline cell number and tapetal identity and promotes seed development in Arabidopsis. Curr. Biol. 12, 1718–1727. Chang, F., Gu, Y., Ma, H., Yang, Z.B., 2013. AtPRK2 promotes ROP1 activation via RopGEFs in the control of polarized pollen tube growth. Mol. Plant 6, 1187– 1201. Chaw, S.M., Chang, C.C., Chen, H.L., Li, W.H., 2004. Dating the monocot-dicot divergence and the origin of core eudicots using whole chloroplast genomes. J. Mol. Evol. 58, 424–441. Chen, Y.H., Zou, M.X., Cao, Y.Y., 2014. Transcriptome analysis of the Arabidopsis semiin vivo pollen tube guidance system uncovers a distinct gene expression profile. J Plant Biol. 57, 93–105. Colcombet, J., Boisson-Dernier, A., Ros-Palau, R., Vera, C.E., Schroeder, J.I., 2005. Arabidopsis somatic embryogenesis receptor kinases 1 and 2 are essential for tapetum development and microspore maturation. Plant Cell 17, 3350–3361. Dai, N., Wang, W., Patterson, S.E., Bleecker, A.B., 2013. The TMK subfamily of receptor-like kinases in Arabidopsis display an essential role in growth and a reduced sensitivity to auxin. PLoS One 8, e60990. DeYoung, B.J., Bickle, K.L., Schrage, K.J., Muskett, P., Patel, K., Clark, S.E., 2006. The CLAVATA1-related BAM1, BAM2 and BAM3 receptor kinase-like proteins are required for meristem function in Arabidopsis. Plant J. 45, 1–16. Guyon, V., Tang, W.H., Monti, M., Raiola, A., DeLorenzo, G., McCormick, S., Taylor, L., 2004. Antisense phenotypes reveal a role for SHY, a pollen-specific leucine-rich repeat protein in pollen tube growth. Plant J. 39, 643–654.

69

Higashiyama, T., Hamamura, Y., 2008. Gametophytic pollen tube guidance. Sex Plant Reprod. 21, 17–26. Holub, E., 2001. Arms race is an ancient history in Arabidopsis, the wildflower. Nat. Rev. Genet. 2, 516–527. Hord, C.L., Chen, C., DeYoung, B.J., Clark, S.E., Ma, H., 2006. The BAM1/BAM2 receptor-like kinases are important regulators of Arabidopsis early anther development. Plant Cell 18, 1667–1680. Hord, C.L., Sun, Y.J., Pillitteri, L.J., Torii, K.U., Wang, H., Zhang, S., Ma, H., 2008. Regulation of Arabidopsis early anther development by the mitogen-activated protein kinases, MPK3 and MPK6, and the ERECTA and related receptor-like kinases. Mol. Plant 1, 645–658. Kaothien, P., Ok, S.H., Shuai, B., Wengier, D., Cotter, R., Kelley, D., Kiriakopolos, S., Muschietti, J., McCormick, S., 2005. Kinase partner protein interacts with the LePRK1 and LePRK2 receptor kinases and plays a role in polarized pollen tube growth. Plant J. 42, 492–503. Kim, H.U., Cotter, R., Johnson, S., Senda, M., Dodds, P., Kulikauskas, R., Tang, W., Ezcurra, I., Herzmark, P., McCormick, S., 2002. New pollen-specific receptor kinases identified in tomato, maize and Arabidopsis: the tomato kinases show overlapping but distinct localization patterns on pollen tubes. Plant Mol. Biol. 50, 1–16. Lee, H.S., Karunanandaa, B., McCubbin, A., Gilroy, S., Kao, T.H., 1996. PRK1, a receptorlike kinase of Petunia inflata, is essential for postmeiotic development of pollen. Plant J. 9, 613–624. Leister, D., 2004. Tandem and segmental gene duplication and recombination in the evolution of plant disease resistance genes. Trends Genet. 20, 116–122. Lynch, M., Conery, J.S., 2000. The evolutionary fate and consequences of duplicate genes. Science 290, 1151–1155. Malho, R., Liu, Q., Monteiro, D., Rato, C., Camacho, L., Dinis, A., 2006. Signalling pathways in pollen germination and tube growth. Protoplasma 228, 21–30. Mizuno, S., Osakabe, Y., Maruyama, K., Ito, T., Osakabe, K., Sato, T., Shinozaki, K., Yamaguchi-Shinozaki, K., 2007. Receptor-like protein kinase 2(RPK2) is a novel factor controlling anther development in Arabidopsis thaliana. Plant J. 50, 751– 766. Mu, J.H., Lee, H.S., Kao, T.H., 1994. Characterization of a pollen-expressed receptorlike kinase gene of Petunia inflate and the activity of its encoded kinase. Plant Cell 6, 709–721. Muschietti, J., Dircks, L., Vancanneyt, G., McCormick, S., 1994. LAT52 protein is essential for tomato pollen development: pollen expressing antisense LAT52 RNA hydrates and germinates abnormally and cannot achieve fertilization. Plant J. 6, 321–338. Muschietti, J., Eyal, Y., McCormick, S., 1998. Pollen tube localization implies a role in pollen–pistil interactions for the tomato receptor-like protein kinases LePRK1 and LePRK2. Plant Cell 10, 319–330. Nonomura, K.I., Miyoshi, K., Eiguchi, M., Suzuki, T., Miyao, A., Hirochika, H., Kurata, N., 2003. The MSP1 gene is necessary to restrict the number of cells entering into male and female sporogenesis and to initiate anther wall formation in rice. Plant Cell 15, 1728–1739. Peng, X.J., Zhao, Y., Cao, J.G., Zhang, W., Jiang, H.Y., Li, X.Y., Ma, Q., Zhu, S.W., Cheng, B. J., 2012. CCCH-type zinc finger family in maize: genome-wide identification, classification and expression profiling under abscisic acid and drought treatments. PLoS One 7, e40120. Salem, T.M., Barberini, M.L., Wengier, D., Cabanasa, M.L., Paza, P., Muschietti, J., 2012. Oligomerization studies show that the kinase domain of the tomato pollen receptor kinase LePRK2 is necessary for interaction with LePRK1. Plant Physiol. Biochem. 53, 40–45. Salem, T.M., Mazzella, A., Barberini, M.L., Wengier, D., Motillo, V., Parisi, G., Muschietti, J., 2011. Mutations in two putative phosphorylation motifs in the tomato pollen receptor kinase LePRK2 show antagonistic effects on pollen tube length. J. Biol. Chem. 286, 4882–4891. Sanderson, M.J., 1997. A nonparametric approach to estimating divergence times in the absence of rate constancy. Mol. Biol. Evol. 14, 1218–1231. Sankoff, D., 2001. Gene and genome duplication. Curr. Opin. Genet. Dev. 11, 681–684. Shi, Y.L., Guo, S.D., Zhang, R., Meng, Z.G., Ren, M.Z., 2014. The role of Somatic embryogenesis receptor-like kinase 1 in controlling pollen production of the Gossypi um anther. Mol. Biol. Rep. 41, 411–422. Shiu, S.H., Bleecker, A.B., 2001. Receptor-like kinases from Arabidopsis form a monophyletic gene family related to animal receptor kinases. Proc. Natl. Acad. Sci. U. S. A. 98, 10763–10768. Shiu, S.H., Bleecker, A.B., 2003. Expansion of the receptor-like kinase/Pelle gene family and receptor-like proteins in Arabidopsis. Plant Physiol. 132, 530–543. Shiu, S.H., Karlowski, W.M., Pan, R., Tzeng, Y.H., Mayer, K.F., Li, W.H., 2004. Comparative analysis of the receptor-like kinase family in Arabidopsis and rice. Plant Cell 16, 1220–1234. Stein, J.C., Howlett, B., Boyes, D.C., Nasrallah, M.E., 1991. Molecular cloning of a putative receptor protein-kinase gene encoded at the self-incompatibility locus of Brassica oleracea. Proc. Natl. Acad. Sci. U. S. A. 88, 8816–8820. Stone, J.M., Walker, J.C., 1995. Plant protein kinase families and signal transduction. Plant Physiol. 108, 451–457. Takahashi, T., Mu, J.H., Gasch, A., Chua, N.H., 1998. Identification by PCR of receptorlike protein kinases from Arabidopsis flowers. Plant Mol. Biol. 37, 587–596. Takasaki, T., Hatakeyama, K., Suzuki, G., Watanabe, M., Isogaill, A., Hinata, K., 2000. The S receptor kinase determines self-incompatibility in Brassica stigma. Nature 403, 913–916. Tang, W.H., Ezcurra, I., Muschietti, J., McCormick, S., 2002. A cysteine-rich extracellular protein, LAT52, interacts with the extracellular domain of the pollen receptor kinase LePRK2. Plant Cell 14, 2277–2287.

70

D. Wang et al. / Computational Biology and Chemistry 51 (2014) 63–70

Tang, W.H., Kelley, D., Ezcurra, I., Cotter, R., McCormick, S., 2004. LeSTIG1, an extracellular binding partner for the pollen receptor kinases LePRK1 and LePRK2, promotes pollen tube growth in vitro. Plant J. 39, 343–353. Walker, J.C., Zhang, R., 1990. Relationship of a putative receptor protein kinase from maize to the S-locus glycoproteins of Brassica. Nature 345, 743–746. Wan, J., Patel, A., Mathieu, M., Kim, S.Y., Xu, D., Stacey, G.A., 2008. A lectin receptorlike kinase is required for pollen development in Arabidopsis. Plant Mol. Biol. 67, 469–482. Wengier, D., Valsecchi, I., Cabanas, M., Tang, W.H., McCormick, S., Muschietti, J., 2003. The receptor kinses LePRK1 and LePRK2 associate in pollen and when expressed in yeast, but dissociate in the presence of style extract. Proc. Natl. Acad. Sci. U. S. A. 100, 6860–6865. Wengier, D., Mazzella, M., Salem, T., McCormick, S., Muschietti, J., 2010. STIL, a peculiar molecule from styles, specifically dephosphorylates the pollen

receptor kinase LePRK2 and stimulates pollen tube growth in vitro. BMC Plant Biol. 10, 33. Xu, A., Huang, L., 2014. Crystallization and preliminary X-ray crystallographic analysis of the extracellular domain of LePRK2 from Lycopersicon esculentum. Acta Cryst. 70, 240–243. Yu, J., Wang, J., Lin, W., Li, S., Li, H., Zhou, J., Ni, P., Dong, W., Hu, S., Zeng, C., 2005. The genomes of Oryza sativa: a history of duplications. PLoS Biol. 3, e38. Zhang, Y., McCormick, S., 2007. A distinct mechanism regulating a pollen-specific guanine nucleotide exchange factor for the small GTPase Rop in Arabidopsis thaliana. Proc. Nat. Acad. Sci. U. S. A. 104, 18830–18835. Zhao, D.Z., Wang, G.F., Speal, B., Ma, H., 2002. The excess microsporocytes1 gene encodes a putative leucine-rich repeat receptor protein kinase that controls somatic and reproductive cell fates in the Arabidopsis anther. Genes Dev. 16, 2021–2031.