Cytological characterization and allelism testing of anther developmental mutants identified in a screen of maize male sterile lines

G3: Genes, Genomes, Genetics

Volumn 3, Issue 2, 2013, Pages 231-249

  Timofejeva, Ljudmilla ^a,b   Skibbe, David S ^c,f   Lee, Sidae ^a   Golubovskaya, Inna ^a,d   Wang, Rachel ^a,g   Harper, Lisa ^a,e   Walbot, Virginia ^c   Cande, William Zacheus ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b TALLINN UNIVERSITY OF TECHNOLOGY   (Estonia)

^c STANFORD UNIVERSITY   (United States)

^d N I VAVILOV ALL RUSSIAN INSTITUTE OF PLANT GENETIC RESOURCES   (Russian Federation)

^e U S DEPARTMENT OF AGRICULTURE   (United States)

^f SYNGENTA CROP PROTECTION   (United States)

^g INSTITUTE OF PLANT AND MICROBIAL BIOLOGY   (Taiwan)

Author keywords

Acquisition; Anther; Cell fate; Development; Maize; Male sterility

Indexed keywords

ALLELISM; ANTHER; ARTICLE; CELL DIFFERENTIATION; CELL FATE; CYTOLOGY; DEGRADATION; GENETIC ANALYSIS; HISTOLOGY; MAIZE; MALE STERILITY; MUTANT; NONHUMAN; ORTHOLOGY; PHENOTYPE; PLANT GENETICS; PLANT INFERTILITY; SOMATIC CELL; ALLELE; ANTHER DEVELOPMENT; CELL FATE ACQUISITION; CELL PROLIFERATION; CLASSIFICATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; MEIOSIS; MUTATION; PLANT GENE; POLLEN;

ARABIDOPSIS; POACEAE; ZEA MAYS;

VEGETABLE PROTEIN;

ANTHER DEVELOPMENT; CELL FATE ACQUISITION; MAIZE; MALE STERILITY;

ALLELES; CELL PROLIFERATION; GENES, PLANT; MEIOSIS; MUTATION; PLANT PROTEINS; POLLEN; ZEA MAYS;

EID: 84883143811     PISSN: None     EISSN: 21601836     Source Type: Journal    
DOI: 10.1534/g3.112.004465     Document Type: Article

References (67)

1. Abramova, L. I., N. A. Avalkina, E. A. Golubeva, Z. S. Pyzhenkova, and I. N. Golubovskaya, 2003 Synthesis and deposition of callose in anthers and ovules of meiotic mutants of maize (Zea mays). Russ. J. Plant Physiol. 50: 324-329.
2. Agashe, B., C. K. Prasad, and I. Siddiqi, 2002 Identification and analysis of DYAD: a gene required for meiotic chromosome organization and female meiotic progression in Arabidopsis. Development 129: 3935-3943.
3. Ambrose, B. A., D. R. Lerner, P. Ciceri, C. M. Padilla, M. F. Yanofsky et al., 2000 Molecular and genetic analyses of the silky1 gene reveal conservation in floral organ specification between eudicots and monocots. Mol. Cell 5: 569-579.
4. Bhalla, P. L., and M. B. Singh, 2006 Molecular control of stem cell maintenance in shoot apical meristem. Plant Cell Rep. 25: 249-256.
5. Bomblies, K., R. L. Wang, B. A. Ambrose, R. J. Schmidt, R. B. Meeley, et al., 2003 Duplicate FLORICAULA/LEAFY homologs zfl1 and zfl2 control inflorescence architecture and flower patterning in maize. Development 11: 2385-2395.
6. Bommert, P., C. Lunde, J. Nardmann, E. Vollbrecht, M. Running, et al., 2005 thick tassel dwarf1 encodes a putative maize ortholog of the Arabidopsis CLAVATA1 leucine-rich repeat receptor-like kinase. Development 132: 1235-1245.
7. Brutnell, T. P., 2002 Transposon tagging in maize. Funct. Integr. Genomics 2: 4-12.
8. Canales, C., A. M. Bhatt, R. Scott, and H. Dickinson, 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.
9. Candela, H., R. Johnston, A. Gerhold, T. Foster, and S. Hake, 2008 The milkweed pod1 gene encodes a KANADI protein that is required for abaxial/adaxial patterning in maize leaves. Plant Cell 20: 2073-2087.
10. Chang, F., Y. Wang, S. Wang, and H. Ma, 2011 Molecular control of microsporogenesis in Arabidopsis. Curr. Opin. Plant Biol. 14: 66-73. Chang, M. T., and M. G. Neuffer, 1994 Chromosomal behavior during microsoporogenesis, pp. 460-475 in The Maize Handbook, edited by M. Freeling, and V. Walbot. Springer-Verlag, New York.
11. Chang, M. T., and M. G. Neuffer, 1994 Chromosomal behavior during microsoporogenesis, pp. 460-475 in The Maize Handbook, edited by M. Freeling, and V. Walbot. Springer-Verlag, New York.
12. Chaubal, R., C. Zanella, M. R. Trimnell, T. W. Fox, M. C. Albertsen, et al., 2000 Two male-sterile mutants of Zea mays (Poaceae) with an extra cell division in the anther wall. Am. J. Bot. 87: 1193-1201.
13. Chaubal, R., J. R. Anderson, M. R. Trimnell, T. W. Fox, M. C. Albertsen, et al., 2003 The transformation of anthers in the msca1 mutant of maize. Planta 216: 778-788.
14. Che, L., D. Tang, K. Wang, M. Wang, K. Zhu, et al., 2011 OsAM1 is required for leptotene-zygotene transition in rice. Cell Res. 21: 654-665.
15. Chen, X.-Y., and J.-Y. Kim, 2009 Callose synthesis in higher plants. Plant Signal. Behav. 4: 489-492.
16. Cigan, A. M., E. Unger, R.-J. Xu, T. Kendall, and T. W. Fox, 2001 Phenotypic complementation of ms45 maize requires tapetal expression of MS45. Sex. Plant Reprod. 14: 135-142.
17. Davis, G. L., 1966 Systematic Embryology of the Angiosperms. J. Wiley, New York.
18. Dawe, R. K., and M. Freeling, 1990 Clonal analysis of the cell lineages in the male flower of maize. Dev. Biol. 142: 233-245.
19. Dereeper, A., V. Guignon, G. Blanc, S. Audic, S. Buffet,, et al., 2008 Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucl. Acids Res. 36: (Web Server Issue) W465.
20. Dinneny, J. R., D. Weigel, and M. F. Yanofsky, 2006 NUBBIN and JAGGED define stamen and carpel shape in Arabidopsis. Development 133: 1645-1655.
21. Duvick, D. N., 1965 Cytoplasmic pollen sterility in corn, pp. 1-56 in Advances in Genetics 13, edited by E. W. Caspari. Academic Press, New York, London.
22. Edgar, R. C., 2004 MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5: 113.
23. Feng, X., and H. G. Dickinson, 2010a Cell-cell interactions during patterning of the Arabidopsis anther. Biochem. Soc. Trans. 38: 571-576.
24. Feng, X., and H. G. Dickinson, 2010b Tapetal cell fate, lineage and proliferation in the Arabidopsis anther. Development 137: 2409-2416.
25. Fernandes, J., Q. Dong, B. Schneider, D. J. Morrow, G.-L. Nan, et al., 2004 Genome-wide mutagenesis of Zea mays L. using RescueMu transposons. Genome Biol. 5: R82.
26. Ge, X., F. Chang, and H. Ma, 2010 Signaling and transcriptional control of reproductive development in Arabidopsis. Curr. Biol. 20: 988-997.
27. Golubovskaya, I., Z. K. Grebennikova, N. A. Avalkina, and W. F. Sheridan, 1993 The role of the ameiotic1 gene in the initiation of meiosis and in subsequent meiotic events in maize. Genetics 135: 1151-1166.
28. Golubovskaya, I., N. Avalkina, and W. F. Sheridan, 1997 New insights into the role of the maize ameiotic1 locus. Genetics 147: 1339-1350.
29. Hale, C. J., J. L. Stonaker, S. M. Gross, and J. B. Hollick, 2007 A novel Snf2 protein maintains trans-generational regulatory states established by paramutation in maize. PLoS Biol. 5: e275.
30. Hong, L., D. Tang, K. Zhu, K. Wang, M. Li, et al., 2012 Somatic and reproductive cell development in rice anther is regulated by a putative glutaredoxin. Plant Cell 24: 577-588.
31. Hord, C., Y.-J. Sun, L. Pillitteri, K. Torii, H. Wang, et al., 2008 Regulation of Arabidopsis early anther development by the mitogen-activated protein kinases, MPK3 and MPK6, and the ERECTA and related receptor-like kinases. Mol.Plant 1: 645-658.
32. Hsu, S. Y., and P. A. Peterson, 1981 Relative stage duration of microsporogenesis in maize. Iowa State J. Res. 55: 351-373.
33. Husbands, A. Y., D. H. Chitwood, Y. Plavskin, and M. C. Timmermans, 2009 Signals and prepatterns: new insights into organ polarity in plants. Genes Dev. 23: 1986-1997.
34. Ikeda, M., N. Mitsuda, and M. Ohme-Takagi, 2009 Arabidopsis WUSCHEL is a bifunctional transcription factor that acts as a repressor in stem cell regulation and as an activator in floral patterning. Plant Cell 21: 3493-3505.
35. Ito, T., F. Wellmer, H. Yu, P. Das, N. Ito, et al., 2004 The homeotic protein AGAMOUS controls microsporogenesis by regulation of SPOROCYTELESS. Nature 430: 356-360.
36. Ito, T., N. Nagata, Y. Yoshiba, M. Ohme-Takagi, H. Ma, et al., 2007 Arabidopsis MALE STERILITY1 encodes a PHD-type transcription factor and regulates pollen and tapetum development. Plant Cell 19: 3549-3562.
37. Jia, G., X. Liu, H. A. Owen, and D. Zhao, 2008 Signaling of cell fate determination by the TPD1 small protein and EMS1 receptor kinase. Proc. Natl. Acad. Sci. USA 105: 2220-2225.
38. Jones, A. M., 2001 Programmed cell death in development and defense. Plant Physiol. 125: 94-97.
39. Juarez, M. T., R. W. Twigg, and M. Timmermans, 2004 Specification of adaxial cell fate during maize leaf development. Development 131: 4533-4544.
40. Kawanabe, T., T. Ariizumi, M. Kawai-Yamada, H. Uchimiya, and K. Toriyama, 2006 Abolition of the tapetum suicide program ruins microsporogenesis. Plant Cell Physiol. 47: 784-787.
41. Kelliher, T., and V. Walbot, 2011 Emergence and patterning of the five cell types of the Zea mays locule. Dev. Biol. 350: 32-49.
42. Kelliher, T., and V. Walbot, 2012 Hypoxia triggers meiotic fate acquisition in maize. Science 337: 345-348.
43. Lam, E., 2004 Controlled cell death, plant survival and development. Nat. Rev. Mol. Cell Biol. 5: 305-315.
44. Laughnan, J. R., and S. Gabay-Laughnan, 1983 Cytoplasmic male sterility in maize. Annu. Rev. Genet. 17: 27-48.
45. Lenhard, M., A. Bohnert, G. Jürgens, and T. Laux, 2001 Termination of stem cell maintenance in Arabidopsis floral meristems by interactions between WUSCHEL and AGAMOUS. Cell 105: 805-814.
46. Li, N., D. S. Zhang, H. S. Liu, C. S. Yin, X. X. Li, et al., 2006 The rice Tapetum Degeneration Retardation gene is required for tapetum degradation and anther development. Plant Cell 18: 2999-3014.
47. Li, H., Z. Yuan, G. Vizcay-Barrena, C. Yang, W. Liang, et al., 2011 PERSISTENT TAPETAL CELL1 encodes a PHD-finger protein that is required for tapetal cell death and pollen development in rice. Plant Physiol. 156: 615-630.
48. Ma, H., 2005 Molecular genetic analyses of microsporogenesis and microgametogenesis in flowering plants. Annu. Rev. Plant Biol. 56: 393-434.
49. Ma, J., D. Duncan, D. J. Morrow, J. Fernandes, and V. Walbot, 2007 Transcriptome profiling of maize anthers using genetic ablation to analyze pre-meiotic and tapetal cell types. Plant J. 50: 637-648.
50. Ma, J., D. S. Skibbe, J. Fernandes, and V. Walbot, 2008 Male reproductive development: Gene expression profiling of maize anther and pollen ontogeny. Genome Biol. 9: R181.
51. Mercier, R., D. Vezon, E. Bullier, J. C. Motamayor, A. Sellier, et al., 2001 SWITCH1 (SWI1): a novel protein required for the establishment of sister chromatid cohesion and for bivalent formation at meiosis. Genes Dev. 15: 1859-1871.
52. Mizuno, S., Y. Osakabe, K. Maruyama, T. Ito, K. Osakabe, et al., 2007 Receptor-like protein kinase2 (RPK2) is a novel factor controlling anther development in Arabidopsis thaliana. Plant J. 50: 751-766.
53. Murmu, J., M. J. Bush, M. C. DeLong, S. Li, M. Xu, et al., 2010 Arabidopsis basic leucine-zipper transcription factors TGA9 and TGA10 interact with floral glutaredoxins ROXY1 and ROXY2 and are redundantly required for anther development. Plant Physiol. 154: 1492-1504.
54. Nan, G. L., A. Ronceret, R. C. Wang, J. F. Fernandes, W. Z. Cande, et al., 2011 Global transcriptome analysis of two ameiotic1 alleles in maize anthers: defining steps in meiotic entry and progression through prophase I. BMC Plant Biol. 11: 120.
55. Nonomura, K., K. Miyoshi, M. Eiguchi, T. Suzuki, A. Miyao, et al., 2003 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 15: 1728-1739.
56. Nonomura, K., M. Eiguchi, M. Nakano, K. Takashima, N. Komeda, et al., 2011 A novel RNA-recognition-motif protein is required for premeiotic G1/S-phase transition in rice (Oryza sativa L.). PLoS Genet. 7: e1001265.
57. Pawlowski, W. P., M. J. Sheehan, and A. Ronceret, 2007 In the beginning: the initiation of meiosis. Bioessays 29: 511-514.
58. Pawlowski, W. P., C. J. Wang, I. N. Golubovskaya, J. M. Szymaniak, L. Shi, et al., 2009 Maize AMEIOTIC1 is essential for multiple early meiotic processes and likely required for the initiation of meiosis. Proc. Natl. Acad. Sci. USA 106: 3603-3608.
59. Phan, H. A., S. Iacuone, S. F. Li, and R. W. Parish, 2011 The MYB80 transcription factor is required for pollen development and the regulation of tapetal programmed cell death in Arabidopsis thaliana. Plant Cell 23: 2209-2224.
60. Raizada, M. N., G. L. Nan, and V. Walbot, 2001 Somatic and germinal mobility of the RescueMu transposon in transgenic maize. Plant Cell 13: 1587-1608.
61. Roeder, A. H. K., V. Chickarmane, A. Cunha, B. Obara, B. S. Manjunath, et al., 2010 Variability in the control of cell division underlies sepal epidermal patterning in Arabidopsis thaliana. PLoS Biol. 8: e1000367.
62. Sheridan, W. F., N. A. Avalkina, I. I. Shamrov, T. B. Batygina, and I. N. Golubovskaya, 1996 The mac1 gene: Controlling the commitment to the meiotic pathway in maize. Genetics 142: 1009-1020.
63. Sheridan, W. F., E. A. Golubeva, L. I. Abrhamova, and I. N. Golubovskaya, 1999 The mac1 mutation alters the developmental fate of the hypodermal cells and their cellular progeny in the maize anther. Genetics 153: 933-941.
64. Shi, Y., S. Zhao, and J. Yao, 2009 Premature tapetum degeneration: a major cause of abortive pollen development in photoperiod sensitive genic male sterility in rice. J. Integr. Plant Biol. 51: 774-781.
65. Skibbe, D. S., and P. S. Schnable, 2005 Male sterility in maize. Maydica 50: 367-376.
66. Skibbe, D. S., X. Wang, L. A. Borsuk, D. A. Ashlock, D. Nettleton, et al., 2008 Floret-specific differences in gene expression and support for the hypothesis that tapetal degeneration of Zea mays L. occurs via programmed cell death. J. Genet. Genomics 35: 603-616.
67. Smith, L. G., S. Hake, and A. W. Sylvester, 1996 The tangled-1 mutation alters cell division orientations throughout maize leaf development without altering leaf shape. Development 122: 481-489.