8.2
CiteScore
6.6
Impact Factor
Volume 51 Issue 10
Oct.  2024
Turn off MathJax
Article Contents

Dosage effect genes modulate grain development in synthesized Triticum durum-Haynaldia villosa allohexaploid

doi: 10.1016/j.jgg.2024.04.010
Funds:

This work was financially supported by the National Key Research and Development Program of China (Grant No. 2022YFF1002900 and 2020YFE0202900), the National Natural Science Foundation of China (32270576), Jiangsu Provincial Key Research and Development Program (BE2022346), Seed Industry Revitalization Project of Jiangsu Province (JBGS[2021]006 and JBGS[2021]013), the Jiangsu Agricultural Technology System (JATS[2023]422), the Joint Research of Wheat Variety Improvement of Anhui, and Zhongshan Biological Breeding Laboratory (ZSBBL) (ZSBBL-KY2023-02-2).

  • Received Date: 2023-09-02
  • Accepted Date: 2024-04-15
  • Rev Recd Date: 2024-04-15
  • Available Online: 2025-06-06
  • Publish Date: 2024-04-25
  • Polyploidization in plants often leads to increased cell size and grain size, which may be affected by the increased genome dosage and transcription abundance. The synthesized Triticum durum (AABB)-Haynaldia villosa (VV) amphiploid (AABBVV) has significantly increased grain size, especially grain length, than the tetraploid and diploid parents. To investigate how polyploidization affects grain development at the transcriptional level, we perform transcriptome analysis using the immature seeds of T. durum, H. villosa, and the amphiploid. The dosage effect genes are contributed more by differentially expressed genes from genome V of H. villosa. The dosage effect genes overrepresent grain development-related genes. Interestingly, the vernalization gene TaVRN1 is among the positive dosage effect genes in the T. durum-H. villosa and T. turgidum-Ae. tauschii amphiploids. The expression levels of TaVRN1 homologs are positively correlated with the grain size and weight. The TaVRN1-B1 or TaVRN1-D1 mutation shows delayed florescence, decreased cell size, grain size, and grain yield. These data indicate that dosage effect genes could be one of the important explanations for increased grain size by regulating grain development. The identification and functional validation of dosage effect genes may facilitate the finding of valuable genes for improving wheat yield.
  • loading
  • Bhatta, M., Morgounov, A., Belamkar, V., Baenziger, P.S., 2018. Genome-wide association study reveals novel genomic regions for grain yield and yield-related traits in drought-stressed synthetic hexaploid wheat. Int. J. Mol. Sci. 19, 3011.
    Birchler, J.A., Bhadra, U., Bhadra, M.P., Auger, D.L., 2001. Dosage-dependent gene regulation in multicellular eukaryotes: Implications for dosage compensation, aneuploid syndromes, and quantitative traits. Dev. Biol. 234, 275-288.
    Birchler, J.A., Riddle, N.C., Auger, D.L., Veitia, R.A., 2005. Dosage balance in gene regulation: biological implications. Trends in genetics : TIG 21, 219-226.
    Blanco, A., Resta, P., Simeone, R., Parmar, S., Shewry, P., Sabelli, P., Lafiandra, D., 1991. Chromosomal location of seed storage protein genes in the genome of Dasypyrum villosum (L.) Candargy. Theoretical and Applied Genetics. 82, 358-362.
    Chen, P., Zhou, B., Qi, L., Liu, D., 1995. Identification of wheat-Haynaldia villosa amphiploid, addition, substitution and translocation lines by in situ hybridization using biotin-labelled genomic DNA as a probe. Yi Chuan xue bao. 22, 380-386.
    Chen, Y., Song, W., Xie, X., Wang, Z., Guan, P., Peng, H., Jiao, Y., Ni, Z., Sun, Q., Guo, W., 2020. A collinearity-incorporating homology inference strategy for connecting emerging assemblies in the triticeae tribe as a pilot practice in the plant pangenomic era. Mol. Plant 13, 1694-1708.
    Conant, G.C., Birchler, J.A., Pires, J.C., 2014. Dosage, duplication, and diploidization: clarifying the interplay of multiple models for duplicate gene evolution over time. Curr. Opin. Plant Biol. 19, 91-98.
    Dong, G., Ni, Z., Yao, Y., Nie, X., Sun, Q., 2007. Wheat Dof transcription factor WPBF interacts with TaQM and activates transcription of an alpha-gliadin gene during wheat seed development. Plant Mol. Biol. 63, 73-84.
    Dong, Z., Yu, J., Li, H., Huang, W., Xu, L., Zhao, Y., Zhang, T., Xu, W., Jiang, J., Su, Z., et al., 2018. Transcriptional and epigenetic adaptation of maize chromosomes in Oat-Maize addition lines. Nucleic Acids Res. 46, 5012-5028.
    Dvorak, J., Akhunov, E.D., 2005. Tempos of gene locus deletions and duplications and their relationship to recombination rate during diploid and polyploid evolution in the Aegilops-Triticum alliance. Genetics 171, 323-332.
    Feldman, M., Levy, A.A., 2012. Genome evolution due to allopolyploidization in wheat. Genetics 192, 763-774.
    Feldman, M., Liu, B., Segal, G., Abbo, S., Levy, A.A., Vega, J.M., 1997. Rapid elimination of low-copy DNA sequences in polyploid wheat: a possible mechanism for differentiation of homoeologous chromosomes. Genetics 147, 1381-1387.
    Galitski, T., Saldanha, A.J., Styles, C.A., Lander, E.S., Fink, G.R., 1999. Ploidy regulation of gene expression. Science 285, 251-254.
    Gu, Y., Li, W., Jiang, H., Wang, Y., Gao, H., Liu, M., Chen, Q., Lai, Y., He, C., 2017. Differential expression of a WRKY gene between wild and cultivated soybeans correlates to seed size. J. Exp. Bot. 68, 2717-2729.
    Guo, F., Huang, Y., Qi, P., Lian, G., Hu, X., Han, N., Wang, J., Zhu, M., Qian, Q., Bian, H., 2021. Functional analysis of auxin receptor OsTIR1/OsAFB family members in rice grain yield, tillering, plant height, root system, germination, and auxinic herbicide resistance. New Phytol. 229, 2676-2692.
    Guo, L., Ma, M., Wu, L., Zhou, M., Li, M., Wu, B., Li, L., Liu, X., Jing, R., Chen, W., et al., 2022. Modified expression of TaCYP78A5 enhances grain weight with yield potential by accumulating auxin in wheat (Triticum aestivum L.). Plant Biotechnol. J. 20, 168-182.
    Huang, C., Zhang, R., Gui, J., Zhong, Y., Li, L., 2018. The receptor-like kinase AtVRLK1 regulates secondary cell wall thickening. Plant Physiol. 177, 671-683.
    I.W.G.S.C., 2018. Shifting the limits in wheat research and breeding using a fully annotated reference genome. Science 361, eaar7191.
    Jackson, S., Chen, Z.J., 2010. Genomic and expression plasticity of polyploidy. Curr. Opin. Plant Biol. 13, 153-159.
    Jia, M., Li, Y., Wang, Z., Tao, S., Sun, G., Kong, X., Wang, K., Ye, X., Liu, S., Geng, S., et al., 2021. TaIAA21 represses TaARF25-mediated expression of TaERFs required for grain size and weight development in wheat. Plant J. 108, 1754-1767.
    Jiang, X., Song, Q., Ye, W., Chen, Z.J., 2021. Concerted genomic and epigenomic changes accompany stabilization of Arabidopsis allopolyploids. Nat. Ecol. Evol. 5, 1382-1393.
    Jiao, W., Yuan, J., Jiang, S., Liu, Y., Wang, L., Liu, M., Zheng, D., Ye, W., Wang, X., Chen, Z.J., 2018. Asymmetrical changes of gene expression, small RNAs and chromatin in two resynthesized wheat allotetraploids. Plant J. 93, 828-842.
    Jofuku, K.D., Omidyar, P.K., Gee, Z., Okamuro, J.K., 2005. Control of seed mass and seed yield by the floral homeotic gene APETALA2. Proc. Natl. Acad. Sci. U S A. 102, 3117-3122.
    Kane, N.A., Agharbaoui, Z., Diallo, A.O., Adam, H., Tominaga, Y., Ouellet, F., Sarhan, F., 2007. TaVRT2 represses transcription of the wheat vernalization gene TaVRN1. Plant J. 51, 670-680.
    Kawakatsu, T., Takaiwa, F., 2010. Differences in Transcriptional regulatory mechanisms functioning for free lysine content and seed storage protein accumulation in rice grain. Plant Cell Physiol. 51, 1964-1974.
    Khaksar, G., Sangchay, W., Pinsorn, P., Sangpong, L., Sirikantaramas, S., 2019. Genome-wide analysis of the Dof gene family in durian reveals fruit ripening-associated and cultivar-dependent Dof transcription factors. Sci. Rep. 9, 12109.
    Kim, D., Langmead, B., Salzberg, S.L., 2015. HISAT: a fast spliced aligner with low memory requirements. Nat. Methods 12, 357-360.
    Kobayashi, K., Yasuno, N., Sato, Y., Yoda, M., Yamazaki, R., Kimizu, M., Yoshida, H., Nagamura, Y., Kyozuka, J., 2012. Inflorescence meristem identity in rice is specified by overlapping functions of three AP1/FUL-like MADS box genes and PAP2, a SEPALLATA MADS box gene. Plant Cell 24, 1848-1859.
    Lei, L., Li, G., Zhang, H., Powers, C., Fang, T., Chen, Y., Wang, S., Zhu, X., Carver, B.F., Yan, L., 2018. Nitrogen use efficiency is regulated by interacting proteins relevant to development in wheat. Plant Biotechnol. J. 16, 1214-1226.
    Levy, A.A., Feldman, M., 2022. Evolution and origin of bread wheat. Plant Cell 34, 2549-2567.
    Li, A., Liu, D., Wu, J., Zhao, X., Hao, M., Geng, S., Yan, J., Jiang, X., Zhang, L., Wu, J., et al., 2014. mRNA and small RNA transcriptomes reveal insights into dynamic homoeolog regulation of allopolyploid heterosis in nascent hexaploid wheat. Plant cell 26, 1878-1900.
    Li, G., Yu, M., Fang, T., Cao, S., Carver, B.F., Yan, L., 2013. Vernalization requirement duration in winter wheat is controlled by TaVRN-A1 at the protein level. Plant J. 76, 742-753.
    Li, N., Xu, R., Li, Y., 2019. Molecular networks of seed size control in plants. Annu. Rev. Plant Biol. 70, 435-463.
    Liu, D. and Chen, P., 1984. N-banding in Haynaldia villosa and Triticum durum-H. villosa Amphidiploid. Yi Chuan xue bao. 11, 106-108.
    Liu, Q., Han, R., Wu, K., Zhang, J., Ye, Y., Wang, S., Chen, J., Pan, Y., Li, Q., Xu, X., et al., 2018. G-protein βγ subunits determine grain size through interaction with MADS-domain transcription factors in rice. Nat. Commun. 9, 852.
    Liu, Y., Yuan, J., Jia, G., Ye, W., Jeffrey Chen, Z., Song, Q., 2021. Histone H3K27 dimethylation landscapes contribute to genome stability and genetic recombination during wheat polyploidization. Plant J. 105, 678-690.
    Lloyd, A., Blary, A., Charif, D., Charpentier, C., Tran, J., Balzergue, S., Delannoy, E., Rigaill, G., Jenczewski, E., 2018. Homoeologous exchanges cause extensive dosage-dependent gene expression changes in an allopolyploid crop. New Phytol. 217, 367-377.
    Luo, M.C., Deal, K.R., Akhunov, E.D., Akhunova, A.R., Anderson, O.D., Anderson, J.A., Blake, N., Clegg, M.T., Coleman-Derr, D., Conley, E.J., et al., 2009. Genome comparisons reveal a dominant mechanism of chromosome number reduction in grasses and accelerated genome evolution in Triticeae. Proc. Natl. Acad. Sci. U. S. A. 106, 15780-15785.
    Ma, L., Li, T., Hao, C., Wang, Y., Chen, X., Zhang, X., 2016. TaGS5-3A, a grain size gene selected during wheat improvement for larger kernel and yield. Plant Biotechnol. J. 14, 1269-1280.
    Maccaferri, M., Harris, N.S., Twardziok, S.O., Pasam, R.K., Gundlach, H., Spannagl, M., Ormanbekova, D., Lux, T., Prade, V.M., Milner, S.G., et al., 2019. Durum wheat genome highlights past domestication signatures and future improvement targets. Nat. Genet. 51, 885-895.
    Malek, M.A., Ismail, M.R., Rafii, M.Y., Rahman, M., 2012. Synthetic Brassica napus L.: development and studies on morphological characters, yield attributes, and yield. ScientificWorldJournal 2012, 416901.
    Miller, M., Zhang, C., Chen, Z.J., 2012. Ploidy and hybridity effects on growth vigor and gene expression in Arabidopsis thaliana hybrids and their parents. G3 (Bethesda, Md.) 2, 505-513.
    Pang, M., Woodward, A.W., Agarwal, V., Guan, X., Ha, M., Ramachandran, V., Chen, X., Triplett, B.A., Stelly, D.M., Chen, Z.J., 2009. Genome-wide analysis reveals rapid and dynamic changes in miRNA and siRNA sequence and expression during ovule and fiber development in allotetraploid cotton (Gossypium hirsutum L.). Genome Biol. 10, R122.
    Pertea, M., Kim, D., Pertea, GM., Leek, JT., Salzberg, SL., 2016. Transcript-level expression analysis of RNA-seq experiments with HISAT, StringTie and Ballgown. Nat. Protoc. 11:1650-1667.
    Qin, L., Zhao, J., Li, T., Hou, J., Zhang, X., Hao, C., 2017. TaGW2, a good reflection of wheat polyploidization and evolution. Front. Plant Sci. 8, 318.
    Ran, L., Pi, M., Wu, J., Jiang, J., Wang, Y., 2017. A comparative study of the seed structure between resynthesized allotetraploid and their diploid parents. Protoplasma 254, 1079-1089.
    Ren, X., Zhi, L., Liu, L., Meng, D., Su, Q., Batool, A., Ji, J., Song, L., Zhang, N., Guo, L., et al., 2021. Alternative splicing of TaGS3 differentially regulates grain weight and size in bread wheat. Int. J. Mol. Sci. 22, 11692.
    Rice, A., Smarda, P., Novosolov, M., Drori, M., Glick, L., Sabath, N., Meiri, S., Belmaker, J., Mayrose, I., 2019. The global biogeography of polyploid plants. Nat. Ecol. Evol. 3, 265-273.
    Robinson, M.D., McCarthy, D.J., Smyth, G.K., 2010. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26, 139-140.
    Salamini, F., Ozkan, H., Brandolini, A., Schafer-Pregl, R., Martin, W., 2002. Genetics and geography of wild cereal domestication in the near east. Nat. Rev. Genet. 3, 429-441.
    Schilling, S., Pan, S., Kennedy, A., Melzer, R., 2018. MADS-box genes and crop domestication: the jack of all traits. J. Exp. Bot. 69, 1447-1469.
    Schruff, M.C., Spielman, M., Tiwari, S., Adams, S., Fenby, N., Scott, R.J., 2006. The AUXIN RESPONSE FACTOR 2 gene of Arabidopsis links auxin signalling, cell division, and the size of seeds and other organs. Development 133, 251-261.
    Song, Q., Ando, A., Jiang, N., Ikeda, Y., Chen, Z.J., 2020. Single-cell RNA-seq analysis reveals ploidy-dependent and cell-specific transcriptome changes in Arabidopsis female gametophytes. Genome Biol. 21, 178.
    Song, Q., Zhang, T., Stelly, D.M., Chen, Z.J., 2017. Epigenomic and functional analyses reveal roles of epialleles in the loss of photoperiod sensitivity during domestication of allotetraploid cottons. Genome Biol. 18, 99.
    Sun, H., Song, J., Lei, J., Song, X., Dai, K., Xiao, J., Yuan, C., An, S., Wang, H., Wang, X., 2018. Construction and application of oligo-based FISH karyotype of Haynaldia villosa. J. Genet. Genomics 45, 463-466.
    Tekeu, H., Ngonkeu, E.L.M., Belanger, S., Djocgoue, P.F., Abed, A., Torkamaneh, D., Boyle, B., Tsimi, P.M., Tadesse, W., Jean, M., et al., 2021. GWAS identifies an ortholog of the rice D11 gene as a candidate gene for grain size in an international collection of hexaploid wheat. Sci. Rep. 11, 19483.
    Thimm, O., Blasing, O., Gibon, Y., Nagel, A., Meyer, S., Kruger, P., Selbig, J., Muller, L.A., Rhee, S.Y., Stitt, M., 2004. MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J. 37, 914-939.
    Vasudevan, A., Levesque-Lemay, M., Edwards, T., Cloutier, S., 2023. Global transcriptome analysis of allopolyploidization reveals large-scale repression of the D-subgenome in synthetic hexaploid wheat. Commun. Biol. 6, 426.
    Wang, L., Yuan, J., Ma, Y., Jiao, W., Ye, W., Yang, D.L., Yi, C., Chen, Z.J., 2018. Rice interploidy crosses disrupt epigenetic regulation, gene expression, and seed development. Mol. Plant 11, 300-314.
    Wu, M., Chang, J., Han, X., Shen, J., Yang, L., Hu, S., Huang, B.B., Xu, H., Xu, M., Wu, S., et al., 2023. A HD-ZIP transcription factor specifies fates of multicellular trichomes via dosage-dependent mechanisms in tomato. Dev. Cell. 58, 278-288.
    Xie, L., Zhang, Y., Wang, K., Luo, X., Xu, D., Tian, X., Li, L., Ye, X., Xia, X., Li, W., et al., 2021. TaVrt2, an SVP-like gene, cooperates with TaVrn1 to regulate vernalization-induced flowering in wheat. New Phytol. 231, 834-848.
    Xu, S., Dong, Q., Deng, M., Lin, D., Xiao, J., Cheng, P., Xing, L., Niu, Y., Gao, C., Zhang, W., et al., 2021. The vernalization-induced long non-coding RNA VAS functions with the transcription factor TaRF2b to promote TaVRN1 expression for flowering in hexaploid wheat. Mol. Plant 14, 1525-1538.
    Yan, L., Liu, Z., Xu, H., Zhang, X., Zhao, A., Liang, F., Xin, M., Peng, H., Yao, Y., Sun, Q., et al., 2018. Transcriptome analysis reveals potential mechanisms for different grain size between natural and resynthesized allohexaploid wheats with near-identical AABB genomes. BMC Plant Biol. 18, 28.
    Yang, C., Zhao, L., Zhang, H., Yang, Z., Wang, H., Wen, S., Zhang, C., Rustgi, S., von Wettstein, D., Liu, B., 2014. Evolution of physiological responses to salt stress in hexaploid wheat. Proc. Natl. Acad. Sci. U. S. A. 111, 11882-11887.
    Yang, W., Liu, D., Li, J., Zhang, L., Wei, H., Hu, X., Zheng, Y., He, Z., Zou, Y., 2009. Synthetic hexaploid wheat and its utilization for wheat genetic improvement in China. J. Genet. Genomics 36, 539-546.
    Yang, Y., Fanning, L., Jack, T., 2003. The K domain mediates heterodimerization of the Arabidopsis floral organ identity proteins, APETALA3 and PISTILLATA. Plant J. 33, 47-59.
    Zhang A, Li N, Gong L, Gou X, Wang B, Deng X, Li C, Dong Q, Zhang H, Liu B. 2017. Global Analysis of Gene Expression in Response to Whole-Chromosome Aneuploidy in Hexaploid Wheat. Plant Physiol. 175, 828-847.
    Zhang, H., Cui, X., Hou, F., Wang, Y., Wu, T., Liu, Y., Yang, D., Zhang, H., Fu, Y., Zhang, X., et al., 2016. Effects of genome doubling on expression of genes regulating grain size in rice. Yichuan 38, 1102-1111.
    Zhang, J., Zhang, H., Li, S., Li, J., Yan, L., Xia, L., 2021. Increasing yield potential through manipulating of an ARE1 ortholog related to nitrogen use efficiency in wheat by CRISPR/Cas9. J. Integr. Plant Biol. 63, 1649-1663.
    Zhang, X., Wang, H., Sun, H., Li, Y., Feng, Y., Jiao, C., Li, M., Song, X., Wang, T., Wang, Z., et al., 2022a. A chromosome-scale genome assembly of Dasypyrum villosum provides insights into its application as a broad-spectrum disease resistance resource for wheat improvement. Mol. Plant 16:432-451.
    Zhang, Y., Li, Z., Liu, J., Zhang, Y., Ye, L., Peng, Y., Wang, H., Diao, H., Ma, Y., Wang, M., et al., 2022b. Transposable elements orchestrate subgenome-convergent and -divergent transcription in common wheat. Nat. Commun. 13, 6940.
    Zhang, Z., Xun, H., Lv, R., Gou, X., Ma, X., Li, J., Zhao, J., Li, N., Gong, L., Liu, B., 2022. Effects of homoeologous exchange on gene expression and alternative splicing in a newly formed allotetraploid wheat. Plant J. 111, 1267-1282.
  • 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

    Article Metrics

    Article views (0) PDF downloads (0) Cited by ()
    Proportional views
    Related

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return