Abstract
The transfer of sperm cells to the egg cell during pollen germination and pollen tube (PT) growth is an essential process for successful reproduction in higher plants. In this process, proper cell wall assembly and remodeling is important for the normal growth of PTs. The functions of members of the Beta(β)-Expansin (EXPB) family, which encode proteins that loosen cell walls, remain poorly understood. Here, we performed a meta-expression analysis of all OsEXPBs sourced from anatomical samples comprising 22 tissues and/or organs. We identified five pollen-preferred OsEXPBs (i.e., OsEXPB1a, OsEXPB1b, OsEXPB9, OsEXPB10, and OsEXPB13). We also identified gene duplication events that specifically involved pollen-preferred OsEXPBs. Subcellular localization of the OsEXPB proteins was found to match well with their roles as cell wall loosening factors, and these were also visible when in transit through the secretory pathway. Further functional characterization of OsEXPBs using a gene editing system for all five targets after removing probable redundancy revealed that a quintuple expb1a;1b;9;10;13 mutant was sterile due to defects in PT elongation. Taken together, the results of our study suggest that the role of five pollen-preferred OsEXPBs that share common expression patterns is important for normal PT growth in rice.
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The datasets used and/or analysed during the current study available from the corresponding author on reasonable request.
References
Cao P, Renna L, Stefano G, Brandizzi F (2016) SYP73 anchors the ER to the actin cytoskeleton for maintenance of ER integrity and streaming in Arabidopsis. Curr Biol CB 26:3245–3254. https://doi.org/10.1016/j.cub.2016.10.024
Carpita NC (1996) Struture and biogenesis of the cell walls of grasses. Annu Rev Plant Physiol Plant Mol Biol 47:445–476. https://doi.org/10.1146/annurev.arplant.47.1.445
Cosgrove DJ, Bedinger P, Durachko DM (1997) Group I allergens of grass pollen as cell wall-loosening agents. Proc Natl Acad Sci USA 94:6559–6564. https://doi.org/10.1073/pnas.94.12.655
Ding A, Marowa P, Kong Y (2016) Genome-wide identification of the expansin gene family in tobacco (Nicotiana tabacum). Mol Genet Genom 291:1891–1907. https://doi.org/10.1007/s00438-016-1226-8
Duman Z, Eliyahu A, Abu-Abied M, Sadot E (2020) The contribution of cell wall remodeling and signaling to lateral organs formation. Isr J Plant Sci 67:110–127. https://doi.org/10.1163/22238980-20191115
Feng X, Li C, He F et al (2022) Genome-wide identification of Expansin Genes in Wild Soybean (Glycine soja) and functional characterization of Expansin B1 (GsEXPB1) in soybean hair root. Int J Mol Sci 23:5407. https://doi.org/10.3390/ijms23105407
Gilbert HJ, Knox JP, Boraston AB (2013) Advances in understanding the molecular basis of plant cell wall polysaccharide recognition by carbohydrate-binding modules. Curr Opin Struct Biol 23:669–677. https://doi.org/10.1016/j.sbi.2013.05.005
Han Z, Liu Y, Deng X et al (2019) Genome-wide identification and expression analysis of expansin gene family in common wheat (Triticum aestivum L.). BMC Genom 20:101. https://doi.org/10.1186/s12864-019-5455-1
Higgins DG, Thompson JD, Gibson TJ (1996) Using CLUSTAL for multiple sequence alignments. Methods Enzymol 266:383–402. https://doi.org/10.1016/s0076-6879(96)66024-8
Hong W-J, Kim Y-J, Chandran AKN, Jung K-H (2019) Infrastructures of systems biology that facilitate functional genomic study in rice. Rice 12:15. https://doi.org/10.1186/s12284-019-0276-z
Hong W-J, Kim E-J, Yoon J et al (2022) A myosin XI adaptor, TAPE, is essential for pollen tube elongation in rice. Plant Physiol 190:562–575. https://doi.org/10.1093/plphys/kiac299
Hong W-J, Moon H, Shin C, Jung K-H (2024) CAFRI-Arabidopsis: an intuitive web-based functional redundancy inspector in Arabidopsis. J Plant Biol. https://doi.org/10.1007/s12374-024-09421-z
Hu H, Zhang R, Dong S et al (2018a) AtCSLD3 and GhCSLD3 mediate root growth and cell elongation downstream of the ethylene response pathway in Arabidopsis. J Exp Bot 69:1065–1080. https://doi.org/10.1093/jxb/erx470
Hu H, Zhang R, Feng S et al (2018b) Three AtCesA6-like members enhance biomass production by distinctively promoting cell growth in Arabidopsis. Plant Biotechnol J 16:976–988. https://doi.org/10.1111/pbi.12842
Jain M, Nijhawan A, Tyagi AK, Khurana JP (2006) Validation of housekeeping genes as internal control for studying gene expression in rice by quantitative real-time PCR. Biochem Biophys Res Commun 345:646–651. https://doi.org/10.1016/j.bbrc.2006.04.140
Jiang L, Yang S-L, Xie L-F et al (2005) VANGUARD1 encodes a pectin methylesterase that enhances pollen tube growth in the Arabidopsis style and transmitting tract. Plant Cell 17:584–596. https://doi.org/10.1105/tpc.104.027631
Jin K-M, Zhuo R-Y, Xu D et al (2020) Genome-wide identification of the expansin gene family and its potential association with drought stress in Moso Bamboo. Int J Mol Sci 21:9491. https://doi.org/10.3390/ijms21249491
Kim MC, Lee SH, Kim JK et al (2002) Mlo, a modulator of plant defense and cell death, is a novel calmodulin-binding protein. Isolation and characterization of a rice Mlo homologue. J Biol Chem 277:19304–19314. https://doi.org/10.1074/jbc.M108478200
Kim Y-J, Zhang D, Jung K-H (2019) Molecular basis of pollen germination in cereals. Trends Plant Sci 24:1126–1136. https://doi.org/10.1016/j.tplants.2019.08.005
Krishnamurthy P, Hong JK, Kim JA et al (2015) Genome-wide analysis of the expansin gene superfamily reveals Brassica rapa-specific evolutionary dynamics upon whole genome triplication. Mol Genet Genom MGG 290:521–530. https://doi.org/10.1007/s00438-014-0935-0
Kudla U, Qin L, Milac A et al (2005) Origin, distribution and 3D-modeling of Gr-EXPB1, an expansin from the potato cyst nematode Globodera rostochiensis. FEBS Lett 579:2451–2457. https://doi.org/10.1016/j.febslet.2005.03.047
Lee Y, Choi D (2005) Biochemical properties and localization of the β-expansin OsEXPB3 in Rice (Oryza sativa L.). Mol Cells 20:119–126. https://doi.org/10.1016/S1016-8478(23)13207-9
Lee Y, Kende H (2001) Expression of β-expansins is correlated with internodal elongation in deepwater rice. Plant Physiol 127:645–654. https://doi.org/10.1104/pp.010345
Lee HW, Kim J (2013) EXPANSINA17 Up-regulated by LBD18/ASL20 promotes lateral root formation during the auxin response. Plant Cell Physiol 54:1600–1611. https://doi.org/10.1093/pcp/pct105
Lee HW, Kim M-J, Kim NY et al (2013) LBD18 acts as a transcriptional activator that directly binds to the EXPANSIN14 promoter in promoting lateral root emergence of Arabidopsis. Plant J 73:212–224. https://doi.org/10.1111/tpj.12013
Leroux C, Bouton S, Kiefer-Meyer M-C et al (2015) Pectin methylesterase48 is involved in arabidopsis pollen grain germination. Plant Physiol 167:367–380. https://doi.org/10.1104/pp.114.250928
Li L-C, Bedinger PA, Volk C, Jones AD, Cosgrove DJ (2003) Purification and characterization of four beta-expansins (Zea m 1 isoforms) from maize pollen. Plant Physiol 132:2073–2085. https://doi.org/10.1104/pp.103.020024
Ling S, Chen C, Wang Y et al (2015) The mature anther-preferentially expressed genes are associated with pollen fertility, pollen germination and anther dehiscence in rice. BMC Genom 16:101. https://doi.org/10.1186/s12864-015-1305-y
Liu X-L, Liu L, Niu Q-K et al (2011) Male gametophyte defective 4 encodes a rhamnogalacturonan II xylosyltransferase and is important for growth of pollen tubes and roots in Arabidopsis. Plant J Cell Mol Biol 65:647–660. https://doi.org/10.1111/j.1365-313X.2010.04452.x
Liu L, Zheng C, Kuang B, Wei L, Yan L, Wang T (2016) Receptor-like kinase RUPO interacts with potassium transporters to regulate pollen tube growth and integrity in rice. PLoS Genet 12(7):e1006085
Liu W, Xu L, Lin H, Cao J (2021) Two Expansin genes, AtEXPA4 and AtEXPB5, are redundantly required for pollen tube growth and AtEXPA4 is involved in primary root elongation in Arabidopsis thaliana. Genes 12:249. https://doi.org/10.3390/genes12020249
Liu X, Dong S, Miao H et al (2022) Genome-wide analysis of expansins and their role in fruit spine development in cucumber (Cucumis sativus L.). Hortic Plant J 8:757–768. https://doi.org/10.1016/j.hpj.2021.11.004
Lu Y, Liu L, Wang X et al (2016) Genome-wide identification and expression analysis of the expansin gene family in tomato. Mol Genet Genom 291:597–608. https://doi.org/10.1007/s00438-015-1133-4
Lv L-M, Zuo D-Y, Wang X-F et al (2020) Genome-wide identification of the expansin gene family reveals that expansin genes are involved in fibre cell growth in cotton. BMC Plant Biol 20:223. https://doi.org/10.1186/s12870-020-02362-y
Ma N, Wang Y, Qiu S et al (2013) Overexpression of OsEXPA8, a root-specific gene, improves rice growth and root system architecture by facilitating cell extension. PLoS ONE 8:e75997. https://doi.org/10.1371/journal.pone.0075997
McQueen-Mason S, Durachko DM, Cosgrove DJ (1992) Two endogenous proteins that induce cell wall extension in plants. Plant Cell 4:1425–1433. https://doi.org/10.1105/tpc.4.11.1425
Morgante CV, Guimarães PM, Martins AC et al (2011) Reference genes for quantitative reverse transcription-polymerase chain reaction expression studies in wild and cultivated peanut. BMC Res Notes 4:339. https://doi.org/10.1186/1756-0500-4-339
Naito Y, Hino K, Bono H, Ui-Tei K (2015) CRISPRdirect: software for designing CRISPR/Cas guide RNA with reduced offtarget sites. Bioinformatics 31(7):1120–1123. https://doi.org/10.1093/bioinformatics/btu743
Panchy N, Lehti-Shiu M, Shiu S-H (2016) Evolution of gene duplication in plants. Plant Physiol 171:2294–2316. https://doi.org/10.1104/pp.16.00523
Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45. https://doi.org/10.1093/nar/29.9.e45
Rizzon C, Ponger L, Gaut BS (2006) Striking similarities in the genomic distribution of tandemly arrayed genes in Arabidopsis and Rice. PLOS Comput Biol 2:e115. https://doi.org/10.1371/journal.pcbi.0020115
Sampedro J, Cosgrove DJ (2005) The expansin superfamily. Genome Biol 6:242. https://doi.org/10.1186/gb-2005-6-12-242
Santo SD, Vannozzi A, Tornielli GB et al (2013) Genome-wide analysis of the expansin gene superfamily reveals grapevine-specific structural and functional characteristics. PLoS ONE 8:e62206. https://doi.org/10.1371/journal.pone.0062206
Schmid M, Davison TS, Henz SR et al (2005) A gene expression map of Arabidopsis thaliana development. Nat Genet 37:501–506. https://doi.org/10.1038/ng1543
Schmidt R, Schippers JHM, Mieulet D et al (2013) MULTIPASS, a rice R2R3-type MYB transcription factor, regulates adaptive growth by integrating multiple hormonal pathways. Plant J 76:258–273. https://doi.org/10.1111/tpj.12286
Silver N, Best S, Jiang J, Thein SL (2006) Selection of housekeeping genes for gene expression studies in human reticulocytes using real-time PCR. BMC Mol Biol 7:33. https://doi.org/10.1186/1471-2199-7-33
Taylor LP, Hepler PK (1997) Pollen germination and tube growth. Annu Rev Plant Physiol Plant Mol Biol 48:461–491. https://doi.org/10.1146/annurev.arplant.48.1.461
Valdivia ER, Wu Y, Li L-C et al (2007) A group-1 grass pollen allergen influences the outcome of pollen competition in maize. PLoS One 2:e154. https://doi.org/10.1371/journal.pone.0000154
Vo KTX, Kim C-Y, Chandran AKN et al (2015) Molecular insights into the function of ankyrin proteins in plants. J Plant Biol 58:271–284. https://doi.org/10.1007/s12374-015-0228-0
Wang Y, Ma N, Qiu S et al (2014) Regulation of the α-expansin gene OsEXPA8 expression affects root system architecture in transgenic rice plants. Mol Breed 34:47–57. https://doi.org/10.1007/s11032-014-0016-4
Ye S, Wang L, Xie W et al (2009) Expression profile of calcium-dependent protein kinase (CDPKs) genes during the whole lifespan and under phytohormone treatment conditions in rice (Oryza sativa L. ssp. indica). Plant Mol Biol 70:311–325. https://doi.org/10.1007/s11103-009-9475-0
Zhang W, Yan H, Chen W et al (2014) Genome-wide identification and characterization of maize expansin genes expressed in endosperm. Mol Genet Genom MGG 289:1061–1074. https://doi.org/10.1007/s00438-014-0867-8
Zou H, Wenwen Y, Zang G et al (2015) OsEXPB2, a β-expansin gene, is involved in rice root system architecture. Mol Breed 35:41. https://doi.org/10.1007/s11032-015-0203-y
Acknowledgements
This study was supported by National Research Foundation of Korea (NRF) grants funded by the Korean government (Grant Nos. NRF-2021R1A5A1032428 and 2021R1A2C2010448 to K.-H. J.), and a grant from the New Breeding Technologies Development Program (No. RS-2024-00322278 to S.M.) of the Rural Development Administration, Republic of Korea.
Funding
This study was supported by National Research Foundation of Korea (NRF) grants funded by the Korean government (Grant Nos. NRF-2021R1A5A1032428 and 2021R1A2C2010448 to K.-H. J.), and a grant from the New Breeding Technologies Development Program (No. RS-2024-00322278 to S.M.) of the Rural Development Administration, Republic of Korea.
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KHJ designed the research project. SKL, HWL, WJH, EJK, and SM performed experiments. SKL, HWL and WJH analyzed data. SKL and HWL wrote the manuscript.
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Lee, SK., Lee, HW., Hong, WJ. et al. Five Beta-Expansin Genes Sharing Common Expression Patterns are Redundantly Involved in Pollen Tube Growth in Rice (Oryza sativa). J. Plant Biol. (2024). https://doi.org/10.1007/s12374-024-09429-5
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DOI: https://doi.org/10.1007/s12374-024-09429-5