Skip to content
naulon

No retraction, correction or concern found when last checked on Nov 2, 2026.

OsTDL1A binds to the LRR domain of rice receptor kinase MSP1, and is required to limit sporocyte numbers

Xinai Zhao, Justina De Palma, Rowena Oane and 6 more

The Plant Journal · 2008

doi:10.1111/j.1365-313x.2008.03426.x

Abstract

Summary Hybrids lose heterotic yield advantage when multiplied sexually via meiosis. A potential alternative breeding system for hybrids is apospory, where female gametes develop without meiosis. Common among grasses, apospory begins in the nucellus, where aposporous initials (AIs) appear near the sexual megaspore mother cell (MeMC). The cellular origin of AIs is obscure, but one possibility, suggested by the mac1 and msp1 mutants of maize and rice, is that AIs are apomeiotic derivatives of the additional MeMCs that appear when genetic control over sporocyte numbers is relaxed. MULTIPLE SPOROCYTES1 ( MSP1 ) encodes a leucine‐rich‐repeat receptor kinase, which is orthologous to EXS/EMS1 in Arabidopsis. Like mac1 and msp1 , exs / ems1 mutants produce extra sporocytes in the anther instead of a tapetum, causing male sterility. This phenotype is copied in mutants of TAPETUM DETERMINANT1 ( TPD1 ), which encodes a small protein hypothesized to be an extracellular ligand of EXS/EMS1. Here we show that rice contains two TPD1 ‐like genes, OsTDL1A and OsTDL1B . Both are co‐expressed with MSP1 in anthers during meiosis, but only OsTDL1A and MSP1 are co‐expressed in the ovule. OsTDL1A binds to the leucine‐rich‐repeat domain of MSP1 in yeast two‐hybrid assays and bimolecular fluorescence complementation in onion cells; OsTDL1B lacks this capacity. When driven by the maize Ubiquitin1 promoter, RNA interference against OsTDL1A phenocopies msp1 in the ovule but not in the anther. Thus, RNAi produces multiple MeMCs without causing male sterility. We conclude that OsTDL1A binds MSP1 in order to limit sporocyte numbers. OsTDL1A ‐RNAi lines may be suitable starting points for achieving synthetic apospory in rice.

Shown for reading. Its publisher allows quoting it, not republishing it.

References 39

  1. 1.

    Bi XZ, de Palma J, Oane R, Khush GS, Bennett J, Virmani SS, Mau CX, Hardy B. Molecular approaches to fixing the heterozygosity of hybrid rice. Hybrid Rice for Food Security, Poverty Alleviations, and Environmental Protection. Proceedings of the 4th International Symposium on Hybrid Rice. 2003;135-150.

    Not in our library

  2. 2.

    Bicknell RA, Koltunow AM. Understanding apomixis: recent advances and remaining conundrums. Plant Cell. 2004;16:S228-S425.

    Not in our library10.1105/tpc.017921

  3. 3.

    Bracha-Drori K, Shichrur K, Katz A, Oliva M, Angelovici R, Yalovsky S, Ohad N. Detection of protein–protein interactions in plants using bimolecular fluorescence complementation. Plant J. 2004;40:419-427.

    Not in our library10.1111/j.1365-313x.2004.02206.x

  4. 4.

    Brar DS, Elloran RM, Lanuang MC, Tolentino VS, Khush GS. Screening wild species of rice for apomixis. Philipp. J. Crop Sci. 1995;20:6.

    Not in our library

  5. 5.

    Canales C, Bhatt AM, Scott R, Dickinson H. 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.

    Not in our library10.1016/s0960-9822(02)01151-x

  6. 6.

    Carman JG. Asynchronous expression of duplicate genes in angiosperms may cause apomixis, bispory, tetraspory, and polyembryony. Biol. J. Linn. Soc. 1997;61:51-94.

    Not in our library

  7. 7.

    Cornejo MJ, Luth D, Blankenship KM, Anderson OD, Blechl AE. Activity of a maize ubiquitin promoter in transgenic rice. Plant Mol. Biol. 1993;23:567-581.

    Not in our library10.1007/bf00019304

  8. 8.

    Deane C, Salwiński Ł, Xenarios I, Eisenberg D. Protein interactions: two methods for assessment of the reliability of high throughput observations. Mol. Cell Proteomics. 2002;1:349-356.

    Not in our library10.1074/mcp.m100037-mcp200

  9. 9.

    Geldner N, Hyman DL, Wang X, Schumacher K, Chory J. Endosomal signaling of plant steroid receptor kinase BRI1. Genes Dev. 2007;21:1598-1602.

    Not in our library10.1101/gad.1561307

  10. 10.

    Guan JC, Jinn TL, Yeh CH, Feng SP, Chen YM, Lin CY. Characterization of the genomic structures and selective expression profiles of nine class I small heat shock protein genes clustered on two chromosomes in rice (Oryza sativa L.). Plant Mol. Biol. 2004;56:795-809.

    Not in our library10.1007/s11103-004-5182-z

  11. 11.

    He Z, Wang ZY, Li J, Zhu Q, Lamb C, Ronald P, Chory J. Perception of brassinosteroids by the extracellular domain of the receptor kinase BRI1. Science. 2000;288:2360-2363.

    Not in our library10.1126/science.288.5475.2360

  12. 12.

    James P, Halladay J, Craig EA. Genomic libraries and a host strain designed for highly efficient two-hybrid selection in yeast. Genetics. 1996;144:1425-1436.

    Not in our library10.1093/genetics/144.4.1425

  13. 13.

    Ji XM, Raveendran M, Oane R, Ismail A, Lafitte R, Bruskiewich R, Cheng SH, Bennett J. Tissue-specific expression and drought responsiveness of cell-wall invertase genes of rice at flowering. Plant Mol. Biol. 2005;59:945-964.

    Not in our library10.1007/s11103-005-2415-8

  14. 14.

    Ji XM, Van den Ende W, Schroeven L, Clerens S, Geuten K, Cheng S, Bennett J. The rice genome encodes two vacuolar invertases with fructan exohydrolase activity but lacks the related fructan biosynthesis genes of the Pooideae. New Phytol. 2007;173:50-62.

    Not in our library10.1111/j.1469-8137.2006.01896.x

  15. 15.

    Jung KH, Han MJ, Lee YS, Kim YW, Hwang I, Kim MJ, Kim YK, Nahm BH, An G. Rice Undeveloped Tapetum1 is a major regulator of early tapetum development. Plant Cell. 2005;17:2705-2722.

    Not in our library10.1105/tpc.105.034090

  16. 16.

    Kathiresan A, Khush GS, Bennett J. Two rice DMC1 genes are differentially expressed during meiosis and during haploid and diploid mitosis. Sex. Plant Reprod. 2002;14:257-267.

    Not in our library

  17. 17.

    Kessler S, Townsley B, Sinha N. L1 division and differentiation patterns influence shoot apical meristem maintenance. Plant Physiol. 2006;141:1349-1362.

    Not in our library10.1104/pp.105.076075

  18. 18.

    Lenhard M, Laux T. Stem cell homeostasis in the Arabidopsis shoot meristem is regulated by intercellular movement of CLAVATA3 and its sequestration by CLAVATA1. Development. 2003;130:3163-3173.

    Not in our library10.1242/dev.00525

  19. 19.

    Luo M, Bilodeau P, Dennis ES, Peacock WJ, Chaudhury A. Expression and parent-of-origin effects for FIS2, MEA, and FIE in the endosperm and embryo of developing Arabidopsis seeds. Proc. Natl Acad. Sci. USA. 2000;97:10637-10642.

    Not in our library10.1073/pnas.170292997

  20. 20.

    Ma H. Molecular genetic analyses of microsporogenesis and microgametogenesis in flowering plants. Annu. Rev. Plant Biol. 2005;56:393-434.

    Not in our library10.1146/annurev.arplant.55.031903.141717

  21. 21.

    Ma J, Duncan D, Morrow DJ, Fernandes J, Walbot V. Transcriptome profiling of maize anthers using genetic ablation to analyze pre-meiotic and tapetal cell types. Plant J. 2007;50:637-648.

    Not in our library10.1111/j.1365-313x.2007.03074.x

  22. 22.

    Matzk F, Prodanovic S, Ba̋umlein H, Schubert I. The Inheritance of apomixis in Poa pratensis confirms a five locus model with differences in gene expressivity and penetrance. Plant Cell. 2005;17:13-24.

    Not in our library10.1105/tpc.104.027359

  23. 23.

    Miki D, Shimamoto K. Simple RNAi vectors for stable and transient suppression of gene function in rice. Plant Cell Physiol. 2004;45:490-495.

    Not in our library10.1093/pcp/pch048

  24. 24.

    Miki D, Itoh R, Shimamoto K. RNA silencing of single and multiple members in a gene family of rice. Plant Physiol. 2005;138:1903-1913.

    Not in our library10.1104/pp.105.063933

  25. 25.

    Ni J, Clark SE. Evidence for functional conservation, sufficiency, and proteolytic processing of the CLAVATA3 CLE domain. Plant Physiol. 2006;140:726-733.

    Not in our library10.1104/pp.105.072678

  26. 26.

    Nielsen H, Engelbrecht J, Brunak S, von Heijne G. A neural network method for identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Int. J. Neural Syst. 1997;8:581-599.

    Not in our library10.1142/s0129065797000537

  27. 27.

    Nonomura K, Miyoshi K, Eiguchi M, Suzuki T, Miyao A, Hirochika H, Kurata N. 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. 2003;15:1728-1739.

    Not in our library10.1105/tpc.012401

  28. 28.

    Page RDM. TREEVIEW: an application to display phylogenetic trees on personal computers. Comput. Appl. Biosci. 1996;12:357-358.

    Not in our library10.1093/bioinformatics/12.4.357

  29. 29.

    Petsalaki EI, Bagos PG, Litou ZI, Hamodrakas SJ. PredSL: a tool for the N-terminal sequence-based prediction of protein subcellular localization. Genomics Proteomics Bioinformatics. 2006;4:48-55.

    Not in our library10.1016/s1672-0229(06)60016-8

  30. 30.

    Russinova E, Borst JW, Kwaaitaal M, Cano-Delgado A, Yin Y, Chory J, de Vries SC. Heterodimerization and endocytosis of Arabidopsis brassinosteroid receptors BRI1 and AtSERK3 (BAK1). Plant Cell. 2004;16:3216-3229.

    Not in our library10.1105/tpc.104.025387

  31. 31.

    Sheridan WF, Avalkina NA, Shamrov II, Batygina TB, Golubovskaya IN. The mac1 gene: controlling the commitment to the meiotic pathway in maize. Genetics. 1996;142:1009-1020.

    Not in our library10.1093/genetics/142.3.1009

  32. 32.

    Sheridan WF, Golubeva EA, Abrhamova LI, Golubovskaya IN. The mac1 mutation alters the developmental fate of the hypodermal cells and their cellular progeny in the maize anther. Genetics. 1999;153:933-941.

    Not in our library10.1093/genetics/153.2.933

  33. 33.

    Streatfield SJ, Magallanes-Lundback ME, Beifuss KK, Brooks CA, Harkey RL, Love RT, Bray J, Howard JA, Jilka JM, Hood EE. Analysis of the maize polyubiquitin-1 promoter heat shock elements and generation of promoter variants with modified expression characteristics. Transgenic Res. 2004;13:299-312.

    Not in our library10.1023/b:trag.0000040053.23687.9c

  34. 34.

    Toki S. Rapid and efficient Agrobacterium-mediated transformation in rice. Plant Mol. Biol. Rep. 1997;15:16-21.

    Not in our library

  35. 35.

    Wang X, Chory J. Brassinosteroids regulate dissociation of BKI1, a negative regulator of BRI1 signaling, from the plasma membrane. Science. 2006;313:1118-1122.

    Not in our library10.1126/science.1127593

  36. 36.

    Wang X, Li X, Meisenhelder J, Hunter T, Yoshida S, Asami T, Chory J. Autoregulation and homodimerization are involved in the activation of the plant steroid receptor BRI1. Dev. Cell. 2005;8:855-865.

    Not in our library10.1016/j.devcel.2005.05.001

  37. 37.

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

    Not in our library10.1105/tpc.016618

  38. 38.

    Yang SL, Jiang LX, Puah CS, Xie LF, Zhang XQ, Chen LQ, Yang WC, Ye D. 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. 2005;139:186-191.

    Not in our library10.1104/pp.105.063529

  39. 39.

    Zhao DZ, Wang GF, Speal B, Ma H. 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. 2002;16:2021-2031.

    Not in our library10.1101/gad.997902

Cited by papers we hold 3

Reads

Read by people on this page

None yet.

Checked or read by AI through naulon

None yet.

A person counts once a day per paper. We keep no cookie and no address: a reader is a hash that changes every day. Any month under five reads shows no number.

Are you an author?

Is this your paper?

Claim it to add your note and be paid when agents cite it. Free.