The non-miR156 targeted SBP-box gene SQUAMOSA PROMOTER BINDING PROTEIN-LIKE 8 ( SPL8), plays an important role in Arabidopsis anther development, where its loss-of-function results in a semi-sterile phenotype. Fully male-sterile plants are obtained when a spl8 loss-of-function mutation is introduced into a 35S:MIR156 genetic background, thereby revealing functional redundancy between SPL8 and miR156-targeted SBP-box genes. Here, we show that BIM1, a gene encoding a bHLH protein involved in brassinosteroid signaling and embryonic patterning, functions redundantly with SPL8 in its requirement for male fertility. Although bim1 single mutants displayed a mild fertility problem due to shortened filaments in some flowers, mutation of BIM1 significantly enhanced the semi-sterile phenotype of the spl8 mutant. Expression of both SPL8 and BIM1 was detected in overlapping expression domains during early anther developmental stages. Our data suggest that in regulating anther development, SPL8 and BIM1 function cooperatively in a common complex or in synergistic pathways. Phylogenetic analysis supports the idea of an evolutionary conserved function for both genes in angiosperm anther development.
References
[1]
Coen, E.S.; Meyerowitz, E.M. The war of the whorls: Genetic interactions controlling flower development. Nature 1991, 353, 31–37, doi:10.1038/353031a0.
[2]
Bowman, J.L.; Baum, S.F.; Eshed, Y.; Putterill, J.; Alvarez, J. Molecular genetics of gynoecium development in Arabidopsis. Curr. Top. Dev. Biol. 1999, 45, 155–205, doi:10.1016/S0070-2153(08)60316-6.
[3]
Scott, R.J.; Spielman, M.; Dickinson, H.G. Stamen structure and function. Plant Cell 2004, 16, S46–S60, doi:10.1105/tpc.017012.
[4]
Causier, B.; Schwarz-Sommer, Z.; Davies, B. Floral organ identity: 20 years of ABCs. Semin. Cell Dev. Biol. 2010, 21, 73–79, doi:10.1016/j.semcdb.2009.10.005.
Ma, H. Molecular genetic analyses of microsporogenesis and microgametogenesis in flowering plants. Annu. Rev. Plant Biol. 2005, 56, 393–434, doi:10.1146/annurev.arplant.55.031903.141717.
[7]
Xing, S.; Salinas, M.; Huijser, P. New players unveiled in early anther development. Plant Signal. Behav. 2011, 6, 934–938, doi:10.4161/psb.6.7.15668.
[8]
Yang, W.C.; Ye, D.; Xu, J.; Sundaresan, V. The SPOROCYTELESS gene of Arabidopsis is required for initiation of sporogenesis and encodes a novel nuclear protein. Genes Dev. 1999, 13, 2108–2117, doi:10.1101/gad.13.16.2108.
[9]
Schiefthaler, U.; Balasubramanian, S.; Sieber, P.; Chevalier, D.; Wisman, E.; Schneitz, K. 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 1999, 96, 11664–11669, doi:10.1073/pnas.96.20.11664.
[10]
Xing, S.; Zachgo, S. ROXY1 and ROXY2, two Arabidopsis glutaredoxin genes, are required for anther development. Plant J. 2008, 53, 790–801, doi:10.1111/j.1365-313X.2007.03375.x.
[11]
Unte, U.S.; Sorensen, A.M.; Pesaresi, P.; Gandikota, M.; Leister, D.; Saedler, H.; Huijser, P. SPL8, an SBP-box gene that affects pollen sac development in Arabidopsis. Plant Cell 2003, 15, 1009–1019, doi:10.1105/tpc.010678.
[12]
Xing, S.; Salinas, M.; H？hmann, S.; Berndtgen, R.; Huijser, P. miR156-targeted and nontargeted SBP-box transcription factors act in concert to secure male fertility in Arabidopsis. Plant Cell 2010, 22, 3935–3950, doi:10.1105/tpc.110.079343.
[13]
Kutschera, U.; Wang, Z.Y. Brassinosteroid action in flowering plants: A darwinian perspective. J. Exp. Bot. 2012, 63, 3511–3522, doi:10.1093/jxb/ers065.
[14]
Ye, Q.; Zhu, W.; Li, L.; Zhang, S.; Yin, Y.; Ma, H.; Wang, X. Brassinosteroids control male fertility by regulating the expression of key genes involved in Arabidopsis anther and pollen development. Proc. Natl. Acad. Sci. USA 2010, 107, 6100–6105.
[15]
Yin, Y.; Vafeados, D.; Tao, Y.; Yoshida, S.; Asami, T.; Chory, J. A new class of transcription factors mediates brassinosteroid-regulated gene expression in Arabidopsis. Cell 2005, 120, 249–259, doi:10.1016/j.cell.2004.11.044.
[16]
Chandler, J.W.; Cole, M.; Flier, A.; Werr, W. BIM1, a bHLH protein involved in brassinosteroid signalling, controls Arabidopsis embryonic patterning via interaction with DORNR？SCHEN and DORNR？SCHEN-LIKE. Plant Mol. Biol. 2009, 69, 57–68, doi:10.1007/s11103-008-9405-6.
[17]
Riese, M.; H？hmann, S.; Saedler, H.; Münster, T.; Huijser, P. Comparative analysis of the SBP-Box gene families in P. patens and seed plants. Gene 2007, 401, 28–37, doi:10.1016/j.gene.2007.06.018.
[18]
Salinas, M.; Xing, S.; H？hmann, S.; Berndtgen, R.; Huijser, P. Genomic organization, phylogenetic comparison and differential expression of the SBP-box family of transcription factors in tomato. Planta 2012, 235, 1171–1184, doi:10.1007/s00425-011-1565-y.
[19]
Pires, N.; Dolan, L. Origin and diversification of basic-helix-loop-helix proteins in plants. Mol. Biol. Evol. 2010, 27, 862–874, doi:10.1093/molbev/msp288.
Zhang, Y. The SBP-box gene SPL8 affects reproductive development and gibberellin response in Arabidopsis. Ph.D. Thesis, University of Cologne, Cologne, Germany, 2005.
Vert, G.; Walcher, C.L.; Chory, J.; Nemhauser, J.L. Integration of auxin and brassinosteroid pathways by Auxin Response Factor 2. Proc. Natl. Acad. Sci. USA 2008, 105, 9829–9834.
[24]
Sundberg, E.; ？stergaard, L. Distinct and dynamic auxin activities during reproductive development. Cold Spring Harb. Perspect. Biol. 2009, 1, a001628, doi:10.1101/cshperspect.a001628.
[25]
Kirch, T.; Simon, R.; Grünewald, M.; Werr, W. The DORNR？SCHEN/ENHANCER OF SHOOT REGENERATION1 gene of Arabidopsis acts in the control of meristem cell fate and lateral organ development. Plant Cell 2003, 15, 694–705, doi:10.1105/tpc.009480.
[26]
Chandler, J.W.; Cole, M.; Flier, A.; Grewe, B.; Werr, W. The AP2 transcription factors DORNR？SCHEN and DORNR？SCHEN-LIKE redundantly control Arabidopsis embryo patterning via interaction with PHAVOLUTA. Development 2007, 134, 1653–1662, doi:10.1242/dev.001016.
[27]
Xing, S.; Rosso, M.G.; Zachgo, S. ROXY1, a member of the plant glutaredoxin family, is required for petal development in Arabidopsis thaliana. Development 2005, 132, 1555–1565, doi:10.1242/dev.01725.
