5.9
CiteScore
5.9
Impact Factor
Volume 47 Issue 8
Aug.  2020
Turn off MathJax
Article Contents

Analyses of functional conservation and divergence reveal requirement of bHLH010/089/091 for pollen development at elevated temperature in Arabidopsis

doi: 10.1016/j.jgg.2020.09.001
More Information
  • The Arabidopsis bHLH010/089/091 (basic helix-loop-helix) genes are functionally redundant and are required for both anther development and normal expression of DYT1-activated anther-related genes. These three genes are conserved in Brassicaceae, suggesting that each of them is under selection pressure; however, little is known about the possible functional differences among these bHLH genes and between the bHLH and DYT1 genes. Here, we compared novel anther transcriptomic data sets from bHLH010/089/091 single and double mutants, with an anther transcriptomic data set from the wild type (WT) and a previously obtained anther transcriptomic data set from the bhlh010 bhlh089 bhlh091 triple mutant. The results revealed molecular phenotypes that support the functional redundancy and divergence of bHLH010, bHLH089, and bHLH091, as well as the functional overlap and difference between them and DYT1. DNA-binding analyses revealed that DYT1 and bHLH089 specifically recognize the TCATGTGC box to activate the expression of target genes, including ATA20, EXL4, and MEE48. In addition, among genes whose expression was affected in the bhlh010 bhlh089 double and bhlh010 bhlh089 bhlh091 triple mutants, genes that are involved in the stress response and cell signaling were enriched, which included 256 genes whose expression was preferentially induced by heat during early flower development. Moreover, the bhlh double mutants exhibited defective pollen development when the plants were grown under elevated temperature, suggesting that bHLH genes are important for anther gene expression under such conditions. These results are consistent with the observation that the heat-induced expression of several genes is less in thebhlh mutants than that in the WT. Therefore, our results provide important insights into the molecular mechanism underlying the activation of direct targets by DYT1-bHLH089 heterodimers and demonstrate the protective roles of bHLH010/089/091 in maintaining fertility upon heat stress.
  • loading
  • [1]
    Canales, C., Bhatt, A.M., Scott, R., Dickinson, H., 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.
    [2]
    Chang, A.T., Liu, Y., Ayyanathan, K., Benner, C., Jiang, Y., Prokop, J.W., Paz, H., Wang, D., Li, H.R., Fu, X.D., Rauscher, F.J., 3rd, Yang, J., 2015. An evolutionarily conserved DNA architecture determines target specificity of the TWIST family bHLH transcription factors. Genes Dev. 29, 603-616.
    [3]
    Chang, F., Wang, Y., Wang, S., Ma, H., 2011. Molecular control of microsporogenesis in Arabidopsis. Curr. Opin. Plant Biol. 14, 66-73.
    [4]
    Clough, S.J., Bent, A.F., 1998. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743.
    [5]
    Colcombet, J., Boissondernier, A., Rospalau, R., Vera, C.E., Schroeder, J.I., 2005. Arabidopsis SOMATIC EMBRYOGENESIS RECEPTOR KINASES1 and 2 are essential for tapetum development and microspore maturation. Plant Cell 17, 3350-3361.
    [6]
    Cui, J., You, C., Zhu, E., Huang, Q., Ma, H., Chang, F., 2016. Feedback Regulation of DYT1 by Interactions with Downstream bHLH Factors Promotes DYT1 Nuclear Localization and Anther Development. Plant Cell 28, 1078-1093.
    [7]
    Dobritsa, A.A., Geanconteri, A., Shrestha, J., Carlson, A., Kooyers, N., Coerper, D., Urbanczyk-Wochniak, E., Bench, B.J., Sumner, L.W., Swanson, R., Preuss, D., 2011. A large-scale genetic screen in Arabidopsis to identify genes involved in pollen exine production. Plant Physiol. Biochem. 157, 947-970.
    [8]
    Ehlting, J., Sauveplane, V., Olry, A., Ginglinger, J.F., Provart, N.J., Werck-Reichhart, D., 2008. An extensive (co-)expression analysis tool for the cytochrome P450 superfamily in Arabidopsis thaliana. BMC Plant Biol. 8, 47.
    [9]
    Ellenberger, T., Fass, D., Arnaud, M., Harrison, S.C., 1994. Crystal structure of transcription factor E47: E-box recognition by a basic region helix-loop-helix dimer. Genes Dev. 8, 970-980.
    [10]
    Feng, B., Lu, D., Ma, X., Peng, Y., Sun, Y., Ning, G., Ma, H., 2012a. Regulation of the Arabidopsis anther transcriptome by DYT1 for pollen development. Plant J. 72, 612-624.
    [11]
    Feng, J., Meyer, C.A., Wang, Q., Liu, J.S., Shirley Liu, X., Zhang, Y., 2012b. GFOLD: a generalized fold change for ranking differentially expressed genes from RNA-seq data. Bioinformatics 28, 2782-2788.
    [12]
    Fu, Z.Z., Yu, J., Cheng, X.W., Zong, X., Xu, J., Chen, M.J., Li, Z.Y., Zhang, D.B., Liang, W.Q., 2014. The Rice Basic Helix-Loop-Helix Transcription Factor TDR INTERACTING PROTEIN2 Is a Central Switch in Early Anther Development. Plant Cell 26, 1512-1524.
    [13]
    Ge, X., Chang, F., Ma, H., 2010. Signaling and transcriptional control of reproductive development in Arabidopsis. Curr. Biol. 20, R988-997.
    [14]
    Gu, J.N., Zhu, J., Yu, Y., Teng, X.D., Lou, Y., Xu, X.F., Liu, J.L., Yang, Z.N., 2014. DYT1 directly regulates the expression of TDF1 for tapetum development and pollen wall formation in Arabidopsis. Plant J. 80, 1005-1013.
    [15]
    Hellens, R.P., Allan, A.C., Friel, E.N., Bolitho, K., Grafton, K., Templeton, M.D., Karunairetnam, S., Gleave, A.P., Laing, W.A., 2005. Transient expression vectors for functional genomics, quantification of promoter activity and RNA silencing in plants. Plant Methods 1, 13.
    [16]
    Hord, C.L., Sun, Y., Pillitteri, L.J., Torii, K.U., Wang, H., Zhang, S., Ma, H., 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.
    [17]
    Huffman, J.L., Mokashi, A., Bachinger, H.P., Brennan, R.G., 2001. The basic helix-loop-helix domain of the aryl hydrocarbon receptor nuclear transporter (ARNT) can oligomerize and bind E-box DNA specifically. J. Biol. Chem. 276, 40537-40544.
    [18]
    Ito, T., Nagata, N., Yoshiba, Y., Ohme-Takagi, M., Ma, H., Shinozaki, K., 2007. Arabidopsis MALE STERILITY1 encodes a PHD-type transcription factor and regulates pollen and tapetum development. Plant Cell 19, 3549-3562.
    [19]
    Ito, T., Shinozaki, K., 2002. The MALE STERILITY1 gene of Arabidopsis, encoding a nuclear protein with a PHD-finger motif, is expressed in tapetal cells and is required for pollen maturation. Plant Cell Physiol. 43, 1285-1292.
    [20]
    Jung, K.H., Han, M.J., Lee, Y.S., Kim, Y.W., Hwang, I.W., Kim, M.J., Kim, Y.K., Nahm, B.H., An, G.H., 2005. Rice Undeveloped Tapetum1 is a major regulator of early tapetum development. Plant Cell 17, 2705-2722.
    [21]
    Lai, C.P., Huang, L.M., Chen, L.O., Chan, M.T., Shaw, J.F., 2017. Genome-wide analysis of GDSL-type esterases/lipases in Arabidopsis. Plant Mol. Biol. 95, 181-197.
    [22]
    Lesk, C., Rowhani, P., Ramankutty, N., 2016. Influence of extreme weather disasters on global crop production. Nature 529, 84-87.
    [23]
    Li, H., Yuan, Z., Vizcay-Barrena, G., Yang, C., Liang, W., Zong, J., Wilson, Z.A., Zhang, D., 2011. PERSISTENT TAPETAL CELL1 encodes a PHD-finger protein that is required for tapetal cell death and pollen development in rice. Plant Physiol. Biochem. 156, 615-630.
    [24]
    Li, N., Zhang, D.S., Liu, H.S., Yin, C.S., Li, X.X., Liang, W.Q., Yuan, Z., Xu, B., Chu, H.W., Wang, J., Wen, T.Q., Huang, H., Luo, D., Ma, H., Zhang, D.B., 2006a. The rice tapetum degeneration retardation gene is required for tapetum degradation and anther development. Plant Cell 18, 2999-3014.
    [25]
    Li, X., Duan, X., Jiang, H., Sun, Y., Tang, Y., Yuan, Z., Guo, J., Liang, W., Chen, L., Yin, J., Ma, H., Wang, J., Zhang, D., 2006b. Genome-wide analysis of basic/helix-loop-helix transcription factor family in rice and Arabidopsis. Plant Physiol. Biochem. 141, 1167-1184.
    [26]
    Liu, H., Yu, X., Li, K., Klejnot, J., Yang, H., Lisiero, D., Lin, C., 2008. Photoexcited CRY2 interacts with CIB1 to regulate transcription and floral initiation in Arabidopsis. Science 322, 1535-1539.
    [27]
    Ma, H., 2005. Molecular genetic analyses of microsporogenesis and microgametogenesis in flowering plants. Annu. Rev. Plant Biol. 56, 393-434.
    [28]
    Ma, P.C., Rould, M.A., Weintraub, H., Pabo, C.O., 1994. Crystal structure of MyoD bHLH domain-DNA complex: perspectives on DNA recognition and implications for transcriptional activation. Cell 77, 451-459.
    [29]
    Nakagawa, T., Ishiguro, S., Kimura, T., 2009. Gateway vectors for plant transformation. Plant Biotechnol. J. 26, 275-284.
    [30]
    Niu, N., Liang, W., Yang, X., Jin, W., Wilson, Z.A., Hu, J., Zhang, D., 2013. EAT1 promotes tapetal cell death by regulating aspartic proteases during male reproductive development in rice. Nat. Commun. 4, 1445.
    [31]
    Parish, R.W., Li, S.F., 2010. Death of a tapetum: A programme of developmental altruism. Plant Sci. 178, 73-89.
    [32]
    Phan, H.A., Iacuone, S., Li, S.F., Parish, R.W., 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.
    [33]
    Rubinelli, P., Hu, Y., Ma, H., 1998. Identification, sequence analysis and expression studies of novel anther-specific genes of Arabidopsis thaliana. Plant Mol. Biol. 37, 607-619.
    [34]
    Sanders, P.M., Bui, A.Q., Weterings, K., McIntire, K.N., Hsu, Y.-C., Lee, P.Y., Truong, M.T., Beals, T.P., Goldberg, R.B., 1999. Anther developmental defects in Arabidopsis thaliana male-sterile mutants. Sex. Plant Reprod. 11, 297-322.
    [35]
    Sorensen, A.M., Krober, S., Unte, U.S., Huijser, P., Dekker, K., Saedler, H., 2003. The Arabidopsis ABORTED MICROSPORES (AMS) gene encodes a MYC class transcription factor. Plant J. 33, 413-423.
    [36]
    Toledo-Ortiz, G., Huq, E., Quail, P.H., 2003. The Arabidopsis basic/helix-loop-helix transcription factor family. Plant Cell 15, 1749-1770.
    [37]
    Trapnell, C., Pachter, L., Salzberg, S.L., 2009. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25, 1105-1111.
    [38]
    Updegraff, E.P., Zhao, F., Preuss, D., 2009. The extracellular lipase EXL4 is required for efficient hydration of Arabidopsis pollen. Sex. Plant Reprod. 22, 197-204.
    [39]
    Wang, S., Lu, J., Song, X.F., Ren, S.C., You, C., Xu, J., Liu, C.M., Ma, H., Chang, F., 2017. Cytological and Transcriptomic Analyses Reveal Important Roles of CLE19 in Pollen Exine Formation. Plant Physiol. 175, 1186-1202.
    [40]
    Wellmer, F., Riechmann, J.L., Alves-Ferreira, M., Meyerowitz, E.M., 2004. Genome-wide analysis of spatial gene expression in Arabidopsis flowers. Plant Cell 16, 1314-1326.
    [41]
    Wilson, Z.A., Morroll, S.M., Dawson, J., Swarup, R., Tighe, P.J., 2001. The Arabidopsis MALE STERILITY1 (MS1) gene is a transcriptional regulator of male gametogenesis, with homology to the PHD-finger family of transcription factors. Plant J. 28, 27-39.
    [42]
    Wilson Wilson, Z.A., Zhang, D.B., 2009. From Arabidopsis to rice: pathways in pollen development. J. Exp. Bot. 60, 1479-1492.
    [43]
    Wu, H.M., Cheun, A.Y., 2000. Programmed cell death in plant reproduction. Plant Mol. Biol. 44, 267-281.
    [44]
    Xu, J., Ding, Z.W., Vizcay-Barrena, G., Shi, J.X., Liang, W.Q., Yuan, Z., Werck-Reichhart, D., Schreiber, L., Wilson, Z.A., Zhang, D.B., 2014. ABORTED MICROSPORES Acts as a Master Regulator of Pollen Wall Formation in Arabidopsis. Plant Cell 26, 1544-1556.
    [45]
    Xu, J., Yang, C.Y., Yuan, Z., Zhang, D.S., Gondwe, M.Y., Ding, Z.W., Liang, W.Q., Zhang, D.B., Wilson, Z.A., 2010. The ABORTED MICROSPORES Regulatory Network Is Required for Postmeiotic Male Reproductive Development in Arabidopsis thaliana. Plant Cell 22, 91-107.
    [46]
    Yang, S., Xie, L., Mao, H., Puah, C.S., Yang, W., Jiang, L., Sundaresan, V., Ye, D., 2003. TAPETUM DETERMINANT1 is required for cell specialization in the Arabidopsis anther. Plant Cell 15, 2792-2804.
    [47]
    Zhang, S.S., Yang, H.X., Ding, L., Song, Z.T., Ma, H., Chang, F., Liu, J.X., 2017. Tissue-Specific Transcriptomics Reveals an Important Role of the Unfolded Protein Response in Maintaining Fertility upon Heat Stress in Arabidopsis. Plant Cell 29, 1007-1023.
    [48]
    Zhang, W., Sun, Y., Timofejeva, L., Chen, C., Grossniklaus, U., Ma, H., 2006. Regulation of Arabidopsis tapetum development and function by DYSFUNCTIONAL TAPETUM1 (DYT1) encoding a putative bHLH transcription factor. Development 133, 3085-3095.
    [49]
    Zhang, Z.B., Zhu, J., Gao, J.F., Wang, C., Li, H., Li, H., Zhang, H.Q., Zhang, S., Wang, D.M., Wang, Q.X., Huang, H., Xia, H.J., Yang, Z.N., 2007. Transcription factor AtMYB103 is required for anther development by regulating tapetum development, callose dissolution and exine formation in Arabidopsis. Plant J. 52, 528-538.
    [50]
    Zhu, J., Chen, H., Li, H., Gao, J.F., Jiang, H., Wang, C., Guan, Y.F., Yang, Z.N., 2008. Defective in Tapetal Development and Function 1 is essential for anther development and tapetal function for microspore maturation in Arabidopsis. Plant J. 55, 266-277.
    [51]
    Zhu, E., You, C., Wang, S., Cui, J., Niu, B., Wang, Y., Qi, J., Ma, H., Chang, F., 2015. The DYT1-interacting proteins bHLH010, bHLH089 and bHLH091 are redundantly required for Arabidopsis anther development and transcriptome. Plant J 83, 976-990.
    [52]
    Zhu, J., Zhang, G.Q., Chang, Y.H., Li, X.C., Yang, J., Huang, X.Y., Yu, Q.B., Chen, H., Wu, T.L., Yang, Z.N., 2010. AtMYB103 is a crucial regulator of several pathways affecting Arabidopsis anther development. Sci. China Life Sci. 53, 1112-1122.
    [53]
    Zik, M., Irish, V.F., 2003. Global identification of target genes regulated by APETALA3 and PISTILLATA floral homeotic gene action. Plant Cell 15, 207-222.
  • 加载中

Catalog

    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索

    Figures (7)

    Article Metrics

    Article views (56) PDF downloads (4) Cited by ()
    Proportional views
    Related

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return