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Cell wall Glycine-rich Protein2 is involved in tapetal differentiation and pollen maturation

  • Regular Paper — Physiology/Biochemistry/Molecular and Cellular Biology
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  • volume 133, pages 883–895 (2020)
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Abstract

The tapetum plays important roles in anther development by providing materials for pollen-wall formation and nutrients for pollen development. Here, we report the characterization of a male-sterile mutant of glycine-rich protein 2 (OsGRP2), which exhibits irregular cell division and dysfunction of the tapetum. GRP is a cellwall structural protein present in the cell walls of diverse plant species, but its function is unclear in pollen development. We found that few GRP genes are expressed in rice and thus focused on one highly expressed gene, OsGRP2. The tapetal cell walls of an OsGRP2 mutant did not thicken at the pollen mothercell stage, as a result, pollen maturation and fertility rate decreased. High OsGRP2 expression was detected in male-floral organs, and OsGRP2 was distributed in the tapetum. OsGRP2 participated in establishment of the cellwall network during early tapetum development. In conclusion, our results indicate that OsGRP2 plays important roles in the differentiation and function of the tapetum.

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References

  • Albrecht C, Russinova E, Hecht V, Baaijens E, de Vries S (2005) The Arabidopsis thaliana SOMATIC EMBRYOGENESIS RECEPTOR-LIKE KINASES1 and 2 control male sporogenesis. Plant Cell 12:3337–3349

    Article  CAS  Google Scholar 

  • Bhatnagar SP, Dantu PK, Bhojwani SS (2018) The Embryology of Angiosperms, 6th edn. Vikas, New Delhi

    Google Scholar 

  • Brutus A, Sicilia F, Macone A, Cervone F, De Lorenzo G (2010) A domain swap approach reveals a role of the plant wall-associated kinase 1 (WAK1) as a receptor of oligogalacturonides. Proc Natl Acad Sci USA 107:9452–9457

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Canales C, Bhatt AM, 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

    Article  CAS  PubMed  Google Scholar 

  • Cankar K, Kortstee A, Toonen MA, Wolters-Arts M, Houbein R, Mariani C, Ulvskov P, Jorgensen B, Schols HA, Visser RG, Trindade LM (2014) Pectic arabinan side chains are essential for pollen cell wall integrity during pollen development. Plant Biotechnol J 12:492–502

    Article  CAS  PubMed  Google Scholar 

  • Cassab GI, Varner JE (1988) Cell Wall Proteins. Ann Rev Plant Physiol Plant Mol Biol 39:321–340

    Article  CAS  Google Scholar 

  • Colcombet J, Boisson-Dernier A, Ros-Palau R, Vera CE, Schroeder JI (2005) Arabidopsis SOMATIC EMBRYOGENESIS RECEPTOR KINASES1 and 2 are essential for tapetum development and microspore maturation. Plant Cell 17:3350–3361

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cosgrove DJ (2005) Growth of the plant cell wall. Nat Rev Mol Cell Biol 6:850–861

    Article  CAS  PubMed  Google Scholar 

  • Decreux A, Messiaen J (2005) Wall-associated kinase WAK1 interacts with cell wall pectins in a calcium-induced conformation. Plant Cell Physiol 46:268–278

    Article  CAS  PubMed  Google Scholar 

  • Deng Y, Wang W, Li WQ, Xia C, Liao HZ, Zhang XQ, Ye D (2010) MALE GAMETOPHYTE DEFECTIVE 2, encoding a sialyltransferase-like protein, is required for normal pollen germination and pollen tube growth in Arabidopsis. J Integr Plant Biol 52:829–843

    Article  CAS  PubMed  Google Scholar 

  • Fujita M, Horiuchi Y, Ueda Y, Mizuta Y, Kubo T, Yano K, Yamaki S, Tsuda K, Nagata T, Niihama M, Kato H, Kikuchi S, Hamada K, Mochizuki T, Ishimizu T, Iwai H, Tsutsumi N, Kurata N (2010) Rice expression atlas in reproductive development. Plant Cell Physiol 12:2060–2081

    Article  CAS  Google Scholar 

  • Goldberg RB, Beals TP, Sanders PM (1993) Anther development: basic principles and practical applications. Plant Cell 5:1217–1229

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gothandam KM, Nalini E, Karthikeyan S, Shin JS (2010) OsPRP3, a flower specific proline-rich protein of rice, determines extracellular matrix structure of floral organs and its overexpression confers cold-tolerance. Plant Mol Biol 72:125–135

    Article  CAS  PubMed  Google Scholar 

  • Hamada K, Hongo K, Suwabe K, Shimizu A, Nagayama T, Abe R, Kikuchi S, Yamamoto N, Fujii T, Yokoyama K, Tsuchida H, Sano K, Mochizuki T, Oki N, Horiuchi Y, Fujita M, Watanabe M, Matsuoka M, Kurata N, Yano K (2011) OryzaExpress: an integrated database of gene expression networks and omics annotations in rice. Plant Cell Physiol 52:220–229

    Article  CAS  PubMed  Google Scholar 

  • Holland PM, Abramson RD, Watson R, Gelfand DH (1991) Detection of specific polymerase chain reaction product by utilizing the 5’----3’ exonuclease activity of Thermus aquaticus DNA polymerase. Proc Natl Acad Sci USA 88:7276–7280

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hord CL, Chen C, Deyoung BJ, Clark SE, Ma H (2006) The BAM1/BAM2 receptor-like kinases are important regulators of Arabidopsis early anther development. Plant Cell 18:1667–1680

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hoshikawa K (1989) The Growing Rice Plant. An anatomical monograph. 282–283

  • Itoh J, Nonomura K, Ikeda K, Yamaki S, Inukai Y, Yamagishi H, Kitano H, Nagato Y (2005) Rice plant development: from zygote to spikelet. Plant Cell Physiol 46:23–47

    Article  CAS  PubMed  Google Scholar 

  • Iwai H, Kikuchi A, Kobayashi T, Kamada H, Satoh S (1999) High levels of non-methylesterified pectins and low levels of peripherally located pectins in loosely attached non-embryogenic callus of carrot. Plant Cell Rep 18:561–566

    Article  CAS  Google Scholar 

  • Iwai H, Hokura A, Oishi M, Chida H, Ishii T, Sakai S, Satoh S (2006) The gene responsible for borate cross-linking of pectin Rhamnogalacturonan-II is required for plant reproductive tissue development and fertilization. Proc Natl Acad Sci USA 103:16592–16597

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jia DJ, Cao X, Wang W, Tan XY, Zhang XQ, Chen LQ, Ye D (2009) GNOM-LIKE 2, encoding an adenosine diphosphate‐ribosylation factor‐guanine nucleotide exchange factor protein homologous to GNOM and GNL1, is essential for pollen germination in Arabidopsis. J Integr Plant Biol 51:762–773

    Article  CAS  PubMed  Google Scholar 

  • Jiang L, Yang SL, Xie LF, Puah CS, Zhang XQ, Yang WC, Sundaresan V, Ye D (2005) VANGUARD1 encodes a pectin methylesterase that enhances pollen tube growth in the Arabidopsis style and transmitting tract. Plant Cell 17:584–596

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Keller B, Sauer N, Lamb CJ (1988) Glycine-rich cell wall proteins in bean: gene structure and association of the protein with the vascular system. EMBO J 7:3625–3633

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lamport DTA (1965) The protein component of primery cell walls. Adv Bot Res 15:151–218

    Google Scholar 

  • Luft LH (1971) Ruthenium red and violet. I. Chemistry, purification, methods of use for electron microscopy and mechanism of action. Anat Rec 171:368

    Google Scholar 

  • Mangeon A, Magioli C, Menezes-Salgueiro AD, Cardeal V, de Oliveira C, Galvão VC, Margis R, Engler G, Sachetto-Martins G (2009) AtGRP5, a vacuole-located glycine-rich protein involved in cell elongation. Planta 230:253–265

    Article  CAS  PubMed  Google Scholar 

  • Mangeon A, Junqueira R, Sachetto-Martins G (2010) Functional diversity of the plant glycine-rich proteins superfamily. Plant Signal Behav 5:99–104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mariani C, De Beuckeleer M, Truettner J, Leemans J, Goldberg RB (1990) Induction of male sterility in plants by a chimeric ribonuclease gene. Nature 347:737–741

    Article  CAS  Google Scholar 

  • Mayfield JA, Preuss D, Rapid (2000) Initiation of Arabidopsis pollination requires the oleosin-domain protein GRP17. Nat Cell Biol 2:128–130

    Article  CAS  PubMed  Google Scholar 

  • McNeil KJ, Smith AG (2010) A glycine-rich protein that facilitates exine for mation during tomato pollen development. Planta 231:793–808

    Article  CAS  PubMed  Google Scholar 

  • Meadows MG (1984) A batch assay using Calcofluor fluorescence to characterize cell wall regeneration in plant protoplasts. Analytical Biochem 141:38–42

    Article  CAS  Google Scholar 

  • Millar AA, Gubler F (2005) The Arabidopsis GAMYB-like genes, MYB33 and MYB65, are microRNA-regulated genes that redundantly facilitate anther development. Plant Cell 17:705–721

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mousavi A, Hiratsuka R, Takase H, Hiratsuka K, Hotta Y (1999) A novel glycine-rich protein is associated with starch grain accumulation during anther development. Plant Cell Physiol 40:406–416

    Article  CAS  PubMed  Google Scholar 

  • Wang N, Huang HJ, Ren ST, Li JJ, Sun Y, Sun DY, Zang SQ (2012) The rice wall-associated receptor-like kinase gene OsDEES1 plays a role in female gametophyte development. Plant Physiol 160:696–707

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pacini E, Franchi GG, Hesse M (1985) The tapetum: its form, function, and possible phylogeny in Embryophyta. Plant Syst Evol 149:155–185

    Article  Google Scholar 

  • Park AR, Cho SK, Yun UJ, Jin MY, Lee SH, Sachetto-Martins G, Park OK (2001) Interaction of the Arabidopsis receptor protein kinase Wak1 with a glycine-rich protein, AtGRP-3. J Biol Chem 276:26688–26693

    Article  CAS  PubMed  Google Scholar 

  • Piffanelli P, Ross JHE, Murphy DJ (1998) Biogenesis and function of the lipidic structures of pollen grains. Sex Plant Reprod 11:65–80

    Article  CAS  Google Scholar 

  • Ringli C, Hauf G, Keller B (2001) Hydrophobic interactions of the structural protein GRP1.8 in the cell wall of protoxylem elements. Plant Physiol 125:673–682

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sachetto-Martins G, Franco L, de Oliveira D (2000) Plant glycine-rich proteins: a family or just proteins with a common motif? Biochem Biophys Acta 1492:1–14

    CAS  PubMed  Google Scholar 

  • Sanders PM, Bui AQ, Weterings K, McIntire KN, Hsu YC, Lee PY, Truong MT, Beals TP, Goldberg RB (1999) Anther developmental defects in Arabidopsis thaliana male-sterile mutants. Sex Plant Reprod 11:297–322

    Article  CAS  Google Scholar 

  • Sato Y, Namiki N, Takehisa H, Kamatsuki K, Minami H, Ikawa H, Ohyanagi H, Sugimoto K, Itoh J, Antonio B, Nagamura Y (2013) RiceFREND: a platform for retrieving coexpressed gene networks in rice. Nucleic Acids Res 41:1214–1221

    Article  CAS  Google Scholar 

  • Schiefthaler U, Balasubramanian S, Sieber P, Chevalier D, Wismann E, Schneitz K (1999) Molecular analysis of NOZZLE, a gene involved in pattern formation and early sporogenesis during sex organ development in Arabidopsis thaliana. Proc Natl Acad Sci USA 96:11664–11669

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Showalter AM (1993) Structure and function of plant cell wall proteins. Plant Cell 5:9–23

    CAS  PubMed  PubMed Central  Google Scholar 

  • Stieglitz H, Stern H (1973) Regulation of beta-1,3-glucanase activity in developing anthers of Lilium. Dev Biol 34:169–173

    Article  CAS  PubMed  Google Scholar 

  • Sumiyoshi M, Nakamura A, Nakamura H, Hakata M, Ichikawa H, Hirochika H, Ishii T, Satoh S, Iwai H (2013) Increase in cellulose accumulation and improvement of saccharification by overexpression of arabinofuranosidase in rice. PLoS One 8:e78269

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sumiyoshi M, Inamura T, Nakamura A, Aohara T, Ishii T, Satoh S, Iwai H (2015) UDP-arabinopyranose mutase 3 is required for pollen wall morphogenesis in rice (Oryza sativa). Plant Cell Physiol 56:233–241

    Article  CAS  Google Scholar 

  • Tao TY, Ouellet T, Dadej K, Miller SS, Johnson DA, Singh J (2006) Characterization of a novel glycine-rich protein from the cell wall of maize silk tissues. Plant Cell Rep 25:848–858

    Article  CAS  PubMed  Google Scholar 

  • Ueki S, Citovsky V (2002) The systemic movement of a tobamovirus is inhibited by a cadmium-ion-induced glycine-rich protein. Nat Cell Biol 4:478–486

    Article  CAS  PubMed  Google Scholar 

  • Uzair M, Xu D, Schreiber L, Shi J, Liang W, Jung KH, Chen M, Luo Z, Zhang Y, Yu J, Zhang (2020) D. PERSISTENT TAPETAL CELL2 Is Required for Normal Tapetal Programmed Cell Death and Pollen Wall Patterning. Plant Physiol 182:962–976

    Article  CAS  PubMed  Google Scholar 

  • Vogel J (2008) Unique aspects of the grass cell wall. Curr Opin Plant Biol 11:301–307

    Article  CAS  PubMed  Google Scholar 

  • Wagner TA, Kohorn BD (2001) Wall-associated kinases are expressed throughout plant development and are required for cell expansion. Plant Cell 13:303–318

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wolfe KH, Gouy M, Yang YW, Sharp PM, Li WH (1989) Date of the monocot-dicot divergence estimated from chloroplast DNA sequence data. Proc Natl Acad Sci USA 86:6201–6205

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu D, Lei M, Wu R (1995) Expression of the rice Osgrp1 promoter-Gus reporter gene is specifically associated with cell elongation/expansion and differentiation. Plant Mol Biol 28:455–471

    Article  CAS  PubMed  Google Scholar 

  • Yang C, Vizcay-Barrena G, Conner K, Wilson ZA (2007) MALE STERILITY1 is required for tapetal development and pollen wall biosynthesis. Plant Cell 19:3530–3548

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang SL, Jiang L, Puah CS, Xie LF, Zhang XQ, Chen LQ, Yang WC, Ye D (2005) Overexpression of TAPETUM DETERMINANT1 alters the cell fates in the Arabidopsis carpel and tapetum via genetic interaction with excess microsporocytes1/extra sporogenous cells. Plant Physiol 139:186–191

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang SL, Xie LF, Mao HZ, Puah CS, Yang WC, Jiang L, Sundaresan V, Ye D (2003) Tapetum determinant1 is required for cell specialization in the Arabidopsis anther. Plant Cell 15:2792–2804

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang WC, Ye D, Xu J, Sundaresan V (1999) The SPOROCYTELESS gene of Arabidopsis is required for initiation of sporogenesis and encodes a novel nuclear protein. Genes Dev 13:2108–2117

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ye ZH, Varner JE (1991) Tissue-specific expression of cell wall proteins in developing soybean tissues. Plant Cell 3:23–37

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang DB, Wilson ZA (2009) Stamen specification and anther development in rice. Chinese Sci Bull 54:2342–2353

    Article  CAS  Google Scholar 

  • Zhao DZ, Wang GF, 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu Y, Dun X, Zhou Z, Xia S, Yi B, Wen J, Shen J, Ma C, Tu J, Fu T (2010) A separation defect of tapetum cells and microspore mother cells results in male sterility in Brassica napus: the role of abscisic acid in early anther development. Plant Mol Biol 72:111–123

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This work was supported by a Grant-in-Aid for Scientific Research on Priority Areas (18075004 to H. Iwai), a Grant-in-Aid for Scientific Research on Innovative Areas (24114006 to S. Satoh and H. Iwai).

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  1. Naomi Takebe and Hiroaki Iwai contributed equally to this work.

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  1. Faculty of Life and Environmental Sciences, University of Tsukuba, Ibaraki, Tsukuba, 305-8572, Japan

    Naomi Takebe, Atsuko Nakamura, Tomomi Watanabe, Aya Miyashita, Shinobu Satoh & Hiroaki Iwai

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  1. Naomi Takebe
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  2. Atsuko Nakamura
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Correspondence to Hiroaki Iwai.

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Takebe, N., Nakamura, A., Watanabe, T. et al. Cell wall Glycine-rich Protein2 is involved in tapetal differentiation and pollen maturation. J Plant Res 133, 883–895 (2020). https://doi.org/10.1007/s10265-020-01223-x

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