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Distribution of cellulosic wall in the anthers of Arabidopsis during microsporogenesis

Abstract

Key message

Cellulose-specific staining revealed that tapetal cells and microsporocytes lose cellulosic walls before the onset of meiosis. Cellulosic wall degradation in microsporocytes might be independent of tapetal cells (or TPD1).

Abstract

Some cell types in a variety of angiosperms have been reported to lack cell walls. Here, we report that the tapetal cells of the anther of Arabidopsis thaliana did not appear to have a cellulosic wall based on staining with Calcofluor and Renaissance 2200. During sporogenous cell formation, cellulosic wall was present in all anther tissues. However, before meiosis it was almost absent on the tapetal cells and on the microsporocytes. In a sporocyteless/nozzle (spl/nzz) mutant, which lacks several components (microsporocytes, tapetum, middle layer and endothecium), cellulosic wall was detected in all anther cells. In another mutant, tapetum determinant1 (tpd1), which lacks tapetum and has more microsporocytes, cellulosic wall was almost absent on the microsporocytes before meiosis, similar to the wild type. These results suggest that the tapetum cells and microsporocytes lose cellulosic walls during microsporocyte formation, and that cell wall degradation occurs downstream of SPL/NZZ and is independent of TPD1.

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Abbreviations

SPL/NZZ:

SPOROCYTELESS/NOZZLE

TPD1:

TAPETUM DETERMINANT1

References

  1. Albersheim P, Darvill A, Roberts K, Sederoff R, Staehelin A (2010) Plant cell walls. Garland Science, New York

    Google Scholar 

  2. 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 17:3337–3349

    PubMed  Article  CAS  Google Scholar 

  3. Carpita NC, Gibeaut DM (1993) Structural models of primary cell walls in flowering plants: consistency of molecular-structure with the physical-properties of the walls during growth. Plant J 3:1–30

    PubMed  Article  CAS  Google Scholar 

  4. Chang F, Wang YX, Wang SS, Ma H (2011) Molecular control of microsporogenesis in Arabidopsis. Curr Opin Plant Biol 14:66–73

    PubMed  Article  CAS  Google Scholar 

  5. Coimbra S, Almeida J, Junqueira V, Costa ML, Pereira LG (2007) Arabinogalactan proteins as molecular markers in Arabidopsis thaliana sexual reproduction. J Exp Bot 58:4027–4035

    PubMed  Article  CAS  Google Scholar 

  6. 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

    PubMed  Article  CAS  Google Scholar 

  7. Echlin P, Godwin H (1968) The ultrastructure and ontogeny of pollen in Helleborus foetidus L. I. The development of the tapetum and ubisch bodies. J Cell Sci 3:161–174

    PubMed  CAS  Google Scholar 

  8. Francis KE, Lam SY, Copenhaver GP (2006) Separation of Arabidopsis pollen tetrads is regulated by QUARTET1, a pectin methylesterase gene. Plant Physiol 142:1004–1013

    PubMed  Article  CAS  Google Scholar 

  9. Harris K, Crabb D, Young IM, Weaver H, Gilligan CA, Otten W, Ritz K (2002) In situ visualisation of fungi in soil thin sections: problems with crystallisation of the fluorochrome FB 28 (Calcofluor M2R) and improved staining by SCRI Renaissance 2200. Mycol Res 106:293–297

    Article  CAS  Google Scholar 

  10. Hird DL, Worrall D, Hodge R, Smartt S, Paul W, Scott R (1993) The anther-specific protein encoded by the Brassica napus and Arabidopsis thaliana A6 gene displays similarity to beta-1,3-glucanases. Plant J 4:1023–1033

    PubMed  Article  CAS  Google Scholar 

  11. Hughes J, McCully ME (1975) The use of an optical brightener in study of plant structure. Stain Technol 50:319–329

    PubMed  CAS  Google Scholar 

  12. Neelam A, Sexton R (1995) Cellulase (endo beta-1,4 glucanase) and cell wall breakdown during anther development in the sweet pea (Lathyrus odoratus L.): isolation and characterization of partial cDNA clones. J Plant Physiol 146:622–628

    Article  CAS  Google Scholar 

  13. Ogawa M, Kay P, Wilson S, Swain SM (2009) ARABIDOPSIS DEHISCENCE ZONE POLYGALACTURONASE1 (ADPG1), ADPG2, and QUARTET2 are polygalacturonases required for cell separation during reproductive development in Arabidopsis. Plant Cell 21:216–233

    PubMed  Article  CAS  Google Scholar 

  14. Owen HA, Makaroff CA (1995) Ultrastructure of microsporogenesis and microgametogenesis in Arabidopsis thaliana (L.) Heynh. ecotype Wassilewskija (Brassicaceae). Protoplasma 185:7–21

    Article  Google Scholar 

  15. Preuss D, Rhee SY, Davis RW (1994) Tetrad analysis possible in Arabidopsis with mutation of the QUARTET (QRT) genes. Science 264:1458–1460

    PubMed  Article  CAS  Google Scholar 

  16. Rhee SY, Somerville CR (1998) Tetrad pollen formation in quartet mutants of Arabidopsis thaliana is associated with persistence of pectic polysaccharides of the pollen mother cell wall. Plant J 15:79–88

    PubMed  Article  CAS  Google Scholar 

  17. Rhee SY, Osborne E, Poindexter PD, Somerville CR (2003) Microspore separation in the quartet 3 mutants of Arabidopsis is impaired by a defect in a developmentally regulated polygalacturonase required for pollen mother cell wall degradation. Plant Physiol 133:1170–1180

    PubMed  Article  CAS  Google Scholar 

  18. 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 

  19. Sexton R, Delcampillo E, Duncan D, Lewis LN (1990) The purification of an anther cellulase (beta(1:4)4-glucan hydrolase) from Lathyrus odoratus L. and its relationship to the similar enzyme found in abscission zones. Plant Sci 67:169–176

    Article  CAS  Google Scholar 

  20. Smyth DR, Bowman JL, Meyerowitz EM (1990) Early flower development in Arabidopsis. Plant Cell 2:755–767

    PubMed  CAS  Google Scholar 

  21. Steer MW (1977) Differentiation of tapetum in Avena. I. The cell surface. J Cell Sci 25:125–138

    PubMed  CAS  Google Scholar 

  22. Talbott LD, Ray PM (1992) Molecular size and separability features of pea cell wall polysaccharides. Implications for models of primary wall structure. Plant Physiol 98:357–368

    PubMed  Article  CAS  Google Scholar 

  23. Urbanowicz BR, Bennett AB, del Campillo E, Catala C, Hayashi T, Henrissat B, Hofte H, McQueen-Mason SJ, Patterson SE, Shoseyov O, Teeri TT, Rose JKC (2007) Structural organization and a standardized nomenclature for plant endo-1,4-beta-glucanases (cellulases) of glycosyl hydrolase family 9. Plant Physiol 144:1693–1696

    PubMed  Article  CAS  Google Scholar 

  24. Wijeratne AJ, Zhang W, Sun YJ, Liu WL, Albert R, Zheng ZQ, Oppenheimer DG, Zhao DZ, Ma H (2007) Differential gene expression in Arabidopsis wild-type and mutant anthers: insights into anther cell differentiation and regulatory networks. Plant J 52:14–29

    PubMed  Article  CAS  Google Scholar 

  25. 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

    PubMed  Article  CAS  Google Scholar 

  26. Yang SL, Xiea LF, Mao HZ, Puah CS, Yang WC, Jiang LX, Sundaresan V, Ye D (2003) TAPETUM DETERMINANT1 is required for cell specialization in the Arabidopsis anther. Plant Cell 15:2792–2804

    PubMed  Article  CAS  Google Scholar 

  27. 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

    PubMed  Article  CAS  Google Scholar 

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Acknowledgments

This work was supported by MEXT KAKENHI Grant Number 18075005 to N.T. and JSPS KAKENHI Grant Number 12J04382 to Y.M.

Conflict of interest

The authors declare that they have no conflict of interest.

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Correspondence to Nobuhiro Tsutsumi.

Additional information

Communicated by A.-C. Schmit.

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Matsuo, Y., Arimura, Si. & Tsutsumi, N. Distribution of cellulosic wall in the anthers of Arabidopsis during microsporogenesis. Plant Cell Rep 32, 1743–1750 (2013). https://doi.org/10.1007/s00299-013-1487-1

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Keywords

  • Arabidopsis
  • Cell wall
  • Sterility
  • Microsporogenesis
  • Tapetum
  • Cellulose