Skip to main content
Log in

AtMYB103 is a crucial regulator of several pathways affecting Arabidopsis anther development

  • Research Papers
  • Published:
Science China Life Sciences Aims and scope Submit manuscript

Abstract

Previous reports indicated that AtMYB103 has an important role in tapetum development, callose dissolution, and exine formation in A. thaliana anthers. Here, we further characterized its function in anther development by expression pattern analysis, transmission electron microscopy observation of the knockout mutant, and microarray analysis of downstream genes. A total of 818 genes differentially expressed between ms188 and the wild-type were identified by global expression profiling analysis. Functional classification showed that loss-of-function of AtMYB103 impairs cell wall modification, lipid metabolic pathways, and signal transduction throughout anther development. RNA in situ hybridization confirmed that transcription factors acting downstream of AtMYB103 (At1g06280 and At1g02040) were expressed in the tapetum and microspores at later stages, suggesting that they might have important roles in microsporogenesis. These results indicated that AtMYB103 is a crucial regulator of Arabidopsis anther development.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Goldberg R B, Beals T P, Sanders P M. Anther development: basic principles and practical applications. Plant Cell, 1993, 5: 1217–1229 1:STN:280:DyaK2c7gvValsg%3D%3D, 10.1105/tpc.5.10.1217, 8281038

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  2. Sanders P M, Bui A Q, Weterings K, et al. Anther developmental defects in Arabidopsis thaliana malesterile mutants. Sex. Plant Reprod, 1999, 11: 297–322 1:CAS:528:DyaK1MXhvVSjt7w%3D, 10.1007/s004970050158

    Article  CAS  Google Scholar 

  3. McCormick S. Control of male gametophyte development. Plant Cell, 2004, 16: 142–153 10.1105/tpc.016659

    Article  Google Scholar 

  4. Pacini E, Franchi G G, Hesse M. The tapetum: its form, function, and possible phylogeny in Embryophyta. Plant Syst Evol, 1985, 149: 155–185 10.1007/BF00983304

    Article  Google Scholar 

  5. Piffanelli P, Ross J H E, Murphy D J. Biogenesis and function of the lipidic structures of pollen grains. Sex. Plant Reprod, 1998, 11: 65–80 1:CAS:528:DyaK1cXkt1KjsL8%3D, 10.1007/s004970050122

    Article  CAS  Google Scholar 

  6. Stevens V A, Murray B G. Studies on heteromorphic self-incompatibility systems: the cytochemistry and ultrastructure of the tapetum of Primula obconica. J Cell Sci, 1981, 50: 419–431 1:STN:280:DyaL38%2FpvVeisw%3D%3D, 7320074

    PubMed  CAS  Google Scholar 

  7. Canales C, Bhatt A M, Scott R, et al. EXS, a putative LRR receptor kinase, regulates male germline cell number and tapetal identity and promotes seed development in Arabidopsis. Curr Biol, 2002, 12: 1718–1727 1:CAS:528:DC%2BD38Xot1ags7w%3D, 10.1016/S0960-9822(02)01151-X, 12401166

    Article  PubMed  CAS  Google Scholar 

  8. Yang S L, Xie L F, Mao H Z, et al. TAPETUM DETERMINANT 1 is required for cell specialization in the Arabidopsis anther. Plant Cell, 2003, 15: 2792–2804 1:CAS:528:DC%2BD2cXhtVSitw%3D%3D, 10.1105/tpc.016618, 14615601

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  9. Zhao D Z, Wang G F, Speal B, et al. The EXCESS MICROSPOROCYTES 1 gene encodes a putative leucine-rich repeat receptor protein kinase that controls somatic and reproductive cell fates in the Arabidopsis anther. Genes Dev, 2002, 16: 2021–2031 1:CAS:528:DC%2BD38XmtFaksro%3D, 10.1101/gad.997902, 12154130

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  10. Paxson-Sowders D M, Owen H A, Makaroff C A. A comparative ultrastructural analysis of exine pattern development in wild-type Arabidopsis and a mutant defective in pattern formation. Protoplasma, 1997, 198: 53–65 10.1007/BF01282131

    Article  Google Scholar 

  11. Zhang W, Sun Y J, Timofejeva L, et al. Regulation of Arabidopsis tapetum development and function by DYSFUNCTIONAL TAPETUM1 (DYT1) encoding a putative bHLH transcription factor. Development, 2006, 133: 3085–3095 1:CAS:528:DC%2BD28XhtVart77P, 10.1242/dev.02463, 16831835

    Article  PubMed  CAS  Google Scholar 

  12. Zhu J, Chen H, Li H, et al. DEFECTIVE IN TAPETAL DEVELOPMENT AND FUNCTION 1 is essential for anther development and tapetal function for microspore maturation in Arabidopsis. Plant J, 2008, 55: 266–277 1:CAS:528:DC%2BD1cXptlals7o%3D, 10.1111/j.1365-313X.2008.03500.x, 18397379

    Article  PubMed  CAS  Google Scholar 

  13. Sorensen A, Krober S, Unte U S, et al. The Arabidopsis ABORTED MICROSPORES (AMS) gene encodes a MYC class transcription factor. Plant J. 2003, 33: 413–423 1:CAS:528:DC%2BD3sXhslWrsrs%3D, 10.1046/j.1365-313X.2003.01644.x, 12535353

    Article  PubMed  CAS  Google Scholar 

  14. Zhang Z B, Zhu J, Gao J F, et al. Transcription factor AtMYB103 is required for anther development by regulating tapetum development, callose dissolution and exine formation in Arabidopsis. Plant J, 2007, 52: 528–538 1:CAS:528:DC%2BD2sXhtl2jtbfF, 10.1111/j.1365-313X.2007.03254.x, 17727613

    Article  PubMed  CAS  Google Scholar 

  15. Wilson Z A, Morroll S M, Dawson J, et al. The Arabidopsis MALE STERILITY 1 (MS1) gene is a transcriptional regulator of male gametogenesis, with homology to the PHD-finger family of transcription factors. Plant J, 2001, 28: 27–39 1:CAS:528:DC%2BD3MXosVWqsrk%3D, 10.1046/j.1365-313X.2001.01125.x, 11696184

    Article  PubMed  CAS  Google Scholar 

  16. Yang C, Vizcay-Barrena G, Conner K, et al. MALE STERILITY 1 is required for tapetal development and pollen wall biosynthesis. Plant Cell, 2007, 19: 3530–3548 1:CAS:528:DC%2BD1cXns1emtw%3D%3D, 10.1105/tpc.107.054981, 18032629

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  17. Li S F, Higginson T, Parish R W. A novel MYB-related gene from Arabidopsis thaliana expressed in development anthers. Plant Cell Physiol, 1999, 40: 343–347 1:CAS:528:DyaK1MXitVSlt7w%3D, 10353220

    Article  PubMed  CAS  Google Scholar 

  18. Fitzgerald M A, Knox R B. Initiation of primexine in freeze substituted microspores of Brassica campestris. Sex Plant Reprod, 1995, 8: 99–104 10.1007/BF00230896

    Article  Google Scholar 

  19. Paxson-Sowders D M, Owen H A, Makaroff C A. A comparative ultrastructural analysis of exine pattern development in wild-type Arabidopsis and a mutant defective in pattern formation. Protoplasma, 1997, 198: 53–65 10.1007/BF01282131

    Article  Google Scholar 

  20. Guan Y F, Huang X Y, Zhu J, et al. RUPTURED POLLEN GRAIN 1 (RPG1), a member of MtN3/Saliva gene family, is crucial for exine pattern formation and cell integrity of microspores in Arabidopsis thaliana. Plant Physiol, 2008, 147: 852–863 1:CAS:528:DC%2BD1cXnsVyhtLw%3D, 10.1104/pp.108.118026, 18434608

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  21. Winter D, Vinegar B, Nahal H, et al. An “electronic fluorescent pictograph” browser for exploring and analyzing large-scale biological data sets. PLoS One, 2007, 8: e718 10.1371/journal.pone.0000718

    Article  Google Scholar 

  22. Thimm O, Bläsing O, Gibon Y, et al. MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J, 2004, 37: 914–939 1:CAS:528:DC%2BD2cXjtFChu78%3D, 10.1111/j.1365-313X.2004.02016.x, 14996223

    Article  PubMed  CAS  Google Scholar 

  23. Shiu S H, Bleecker A B. Receptor-like kinases from Arabidopsis form a monophyletic gene family related to animal receptor kinases. Proc Natl Acad Sci USA, 2001, 98: 10763–10768 1:CAS:528:DC%2BD3MXntVGms7g%3D, 10.1073/pnas.181141598, 11526204

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  24. Dievart A, Clark S E. LRR-containing receptors regulating plant development and defense. Development, 2004, 131: 251–261 1:CAS:528:DC%2BD2cXhsVSrtLo%3D, 10.1242/dev.00998, 14701679

    Article  PubMed  CAS  Google Scholar 

  25. Cole R, Fowler J. Polarized growth: maintaining focus on the tip. Curr Opin Plant Biol, 2006, 9: 579–588 1:CAS:528:DC%2BD28XhtVygt7vL, 10.1016/j.pbi.2006.09.014, 17010659

    Article  PubMed  CAS  Google Scholar 

  26. Holdaway-Clarke T L, Feijo J A, Hackett G R, et al. Pollen tube growth and the intracellular cytosolic calcium gradient oscillate in phase while extracellular calcium influx is delayed. Plant Cell, 1997, 9: 1999–2010 1:CAS:528:DyaK2sXnsl2mt7o%3D, 10.1105/tpc.9.11.1999, 12237353

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  27. Franklin-Tong V E. Signaling and the modulation of pollen tube growth. Plant Cell, 1999, 11: 727–738 1:CAS:528:DyaK1MXjtFSrurc%3D, 10.1105/tpc.11.4.727, 10213789

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  28. Moutinho A, Trewavas A J, Malho R. Relocation of a Ca2+-dependent protein kinase activity during pollen tube reorientation. Plant Cell, 1998, 10: 1499–1510 1:CAS:528:DyaK1cXmsVKiu7w%3D, 10.1105/tpc.10.9.1499, 9724696

    PubMed  CAS  PubMed Central  Google Scholar 

  29. Kost B, Lemichez E, Spielhofer P, et al. Rac homologues and compartmentalized phosphatidylinositol 4,5-biphosphate act in a common pathway to regulate polar pollen tube growth. J Cell Biol, 1999, 145: 317–330 1:CAS:528:DyaK1MXislSgtL0%3D, 10.1083/jcb.145.2.317, 10209027

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  30. Ischebeck T, Stenzel I, Heilmann I. Type B phosphatidylinositol-4-phosphate 5-kinases mediate Arabidopsis and Nicotiana tabacum pollen tube growth by regulating apical pectin secretion. Plant Cell, 2008, 20: 3312–3330 1:CAS:528:DC%2BD1MXitVarur0%3D, 10.1105/tpc.108.059568, 19060112

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  31. Northcote D H. Chemistry of the plant cell wall. Ann Rev Pl Physiol, 1972, 23: 113–132 1:CAS:528:DyaE38XkvVGmsrs%3D, 10.1146/annurev.pp.23.060172.000553

    Article  CAS  Google Scholar 

  32. Hsieh K, Huang A H. Tapetosomes in Brassica tapetum accumulate endoplasmic reticulum-derived flavonoids and alkanes for delivery to the pollen surface. Plant Cell, 2007, 19: 582–596 1:CAS:528:DC%2BD2sXktFGns7Y%3D, 10.1105/tpc.106.049049, 17307923

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  33. Aarts M G, Hodge R, Kalantidis K, et al. The Arabidopsis MALE STERILITY 2 protein shares similarity with reductases in elongation/condensation complexes. Plant J, 1997, 12: 615–623 1:CAS:528:DyaK2sXntVCktbs%3D, 10.1046/j.1365-313X.1997.d01-8.x, 9351246

    Article  PubMed  CAS  Google Scholar 

  34. Morant M, Jorgensen K, Schaller H, et al. CYP703 is an ancient cytochrome P450 in land plants catalyzing in-chain hydroxylation of lauric acid to provide building blocks for sporopollenin synthesis in pollen. Plant Cell, 2007, 19: 1473–1487 1:CAS:528:DC%2BD2sXnvVWqt7c%3D, 10.1105/tpc.106.045948, 17496121

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  35. Akoh C C, Lee G C, Liaw Y C, et al. GDSL family of serine esterases/lipases. Prog Lipid Res, 2004, 43: 534–552 1:CAS:528:DC%2BD2cXptFKqs7k%3D, 10.1016/j.plipres.2004.09.002, 15522763

    Article  PubMed  CAS  Google Scholar 

  36. Brick D J, Brumlik M J, Buckley J T, et al. A new family of lipolytic plant enzymes with members in rice, Arabidopsis and maize. FEBS Lett, 1995, 377: 475–480 1:CAS:528:DyaK28Xnt1yr, 10.1016/0014-5793(95)01405-5, 8549779

    Article  PubMed  CAS  Google Scholar 

  37. Koltunow A M, Truettner J, Cox K H, et al. Different temporal and spatial gene expression patterns occur during anther development. Plant Cell, 1990, 2: 1201–1224 1:CAS:528:DyaK3MXkvVKnsr4%3D, 10.1105/tpc.2.12.1201, 12354953

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  38. Foster G D, Robinson S W, Blundell R P, et al. A Brassica napus mRNA encoding a protein homologous to phospholipid transfer proteins is expressed specifically in the tapetum and developing microspores. Plant Sci, 1992, 84: 187–192 1:CAS:528:DyaK3sXkt1Clu74%3D, 10.1016/0168-9452(92)90133-7

    Article  CAS  Google Scholar 

  39. Durbarry A, Vizir I, Twell D. Male germ line development in Arabidopsis. duo pollen mutants reveal gametophytic regulators of generative cell cycle progression. Plant Physiol, 2005, 137: 297–307 1:CAS:528:DC%2BD2MXhtFOls7c%3D, 10.1104/pp.104.053165, 15618418

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  40. Alves-Ferreira M, Wellmer F, Banhara A, et al. Global expression profiling applied to the analysis of Arabidopsis stamen development. Plant Physiol, 2007, 145: 747–762 1:CAS:528:DC%2BD2sXhtlemsrnM, 10.1104/pp.107.104422, 17905860

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  41. Adamczyk B J, Fernandez D E. MIKC* MADS domain heterodimers are required for pollen maturation and tube growth in Arabidopsis. Plant Physiol, 2009, 149: 1713–1723 1:CAS:528:DC%2BD1MXks1Wgurw%3D, 10.1104/pp.109.135806, 19211705

    Article  PubMed  CAS  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to TianLong Wu or ZhongNan Yang.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zhu, J., Zhang, G., Chang, Y. et al. AtMYB103 is a crucial regulator of several pathways affecting Arabidopsis anther development. Sci. China Life Sci. 53, 1112–1122 (2010). https://doi.org/10.1007/s11427-010-4060-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11427-010-4060-y

Keywords

Navigation