A Rice Ca2+ Binding Protein Is Required for Tapetum Function and Pollen Formation.
In flowering plants, successful male reproduction requires the sophisticated interaction between somatic anther wall layers and reproductive cells. Timely degradation of the innermost tissue of the anther wall layer, the tapetal layer, is critical for pollen development. Ca2+is a well-known stimulus for plant development, but whether it plays a role in affecting male reproduction remains elusive. Here we report a role of Defective in Exine Formation 1 (OsDEX1) in rice (Oryza sativa), a Ca2+binding protein, in regulating rice tapetal cell degradation and pollen formation. In osdex1 anthers, tapetal cell degeneration is delayed and degradation of the callose wall surrounding the microspores is compromised, leading to aborted pollen formation and complete male sterility. OsDEX1 is expressed in tapetal cells and microspores during early anther development. Recombinant OsDEX1 is able to bind Ca2+and regulate Ca2+homeostasis in vitro, and osdex1 exhibited disturbed Ca2+homeostasis in tapetal cells. Phylogenetic analysis suggested that OsDEX1 may have a conserved function in binding Ca2+in flowering plants, and genetic complementation of pollen wall defects of an Arabidopsis (Arabidopsis thaliana) dex1 mutant confirmed its evolutionary conservation in pollen development. Collectively, these findings suggest that OsDEX1 plays a fundamental role in the development of tapetal cells and pollen formation, possibly via modulating the Ca2+homeostasis during pollen development.
Joint International Research Laboratory of Metabolic & Developmental Sciences, Shanghai Jiao Tong University-University of Adelaide Joint Centre for Agriculture and Health, School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai 200240, China (J.Y., Z.M., W.L., Z.L., M.C., D.X., G.Z., J.W., S.Z., Y.-J.K., D.Z.).|Institut für Biologie und Biotechnologie der Pflanzen, Westfälische Wilhelms-Universität Münster, Schlossplatz 7, 48149 Münster, Germany (J.K.); Department of Oriental Medicinal Biotechnology, College of Life Science, Kyung Hee University, Yongin 446-701, Republic of Korea (Y.-J.K).|Indian Institute of Chemical Biology, Council of Scientific and Industrial Research, 700 032 West Bengal, India (S.B.); and.|School of Agriculture, Food and Wine, University of Adelaide, Waite Campus, Urrbrae, SA 5064, Australia (M.R.T., D.Z.).
Jing
J
Yu
Joint International Research Laboratory of Metabolic & Developmental Sciences, Shanghai Jiao Tong University-University of Adelaide Joint Centre for Agriculture and Health, School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai 200240, China (J.Y., Z.M., W.L., Z.L., M.C., D.X., G.Z., J.W., S.Z., Y.-J.K., D.Z.).|Institut für Biologie und Biotechnologie der Pflanzen, Westfälische Wilhelms-Universität Münster, Schlossplatz 7, 48149 Münster, Germany (J.K.); Department of Oriental Medicinal Biotechnology, College of Life Science, Kyung Hee University, Yongin 446-701, Republic of Korea (Y.-J.K).|Indian Institute of Chemical Biology, Council of Scientific and Industrial Research, 700 032 West Bengal, India (S.B.); and.|School of Agriculture, Food and Wine, University of Adelaide, Waite Campus, Urrbrae, SA 5064, Australia (M.R.T., D.Z.).
Zhaolu
Z
Meng
Joint International Research Laboratory of Metabolic & Developmental Sciences, Shanghai Jiao Tong University-University of Adelaide Joint Centre for Agriculture and Health, School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai 200240, China (J.Y., Z.M., W.L., Z.L., M.C., D.X., G.Z., J.W., S.Z., Y.-J.K., D.Z.).|Institut für Biologie und Biotechnologie der Pflanzen, Westfälische Wilhelms-Universität Münster, Schlossplatz 7, 48149 Münster, Germany (J.K.); Department of Oriental Medicinal Biotechnology, College of Life Science, Kyung Hee University, Yongin 446-701, Republic of Korea (Y.-J.K).|Indian Institute of Chemical Biology, Council of Scientific and Industrial Research, 700 032 West Bengal, India (S.B.); and.|School of Agriculture, Food and Wine, University of Adelaide, Waite Campus, Urrbrae, SA 5064, Australia (M.R.T., D.Z.).
Wanqi
0000-0002-9938-5793
W
Liang
Joint International Research Laboratory of Metabolic & Developmental Sciences, Shanghai Jiao Tong University-University of Adelaide Joint Centre for Agriculture and Health, School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai 200240, China (J.Y., Z.M., W.L., Z.L., M.C., D.X., G.Z., J.W., S.Z., Y.-J.K., D.Z.).|Institut für Biologie und Biotechnologie der Pflanzen, Westfälische Wilhelms-Universität Münster, Schlossplatz 7, 48149 Münster, Germany (J.K.); Department of Oriental Medicinal Biotechnology, College of Life Science, Kyung Hee University, Yongin 446-701, Republic of Korea (Y.-J.K).|Indian Institute of Chemical Biology, Council of Scientific and Industrial Research, 700 032 West Bengal, India (S.B.); and.|School of Agriculture, Food and Wine, University of Adelaide, Waite Campus, Urrbrae, SA 5064, Australia (M.R.T., D.Z.).
Smrutisanjita
S
Behera
Joint International Research Laboratory of Metabolic & Developmental Sciences, Shanghai Jiao Tong University-University of Adelaide Joint Centre for Agriculture and Health, School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai 200240, China (J.Y., Z.M., W.L., Z.L., M.C., D.X., G.Z., J.W., S.Z., Y.-J.K., D.Z.).|Institut für Biologie und Biotechnologie der Pflanzen, Westfälische Wilhelms-Universität Münster, Schlossplatz 7, 48149 Münster, Germany (J.K.); Department of Oriental Medicinal Biotechnology, College of Life Science, Kyung Hee University, Yongin 446-701, Republic of Korea (Y.-J.K).|Indian Institute of Chemical Biology, Council of Scientific and Industrial Research, 700 032 West Bengal, India (S.B.); and.|School of Agriculture, Food and Wine, University of Adelaide, Waite Campus, Urrbrae, SA 5064, Australia (M.R.T., D.Z.).
Jörg
J
Kudla
Joint International Research Laboratory of Metabolic & Developmental Sciences, Shanghai Jiao Tong University-University of Adelaide Joint Centre for Agriculture and Health, School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai 200240, China (J.Y., Z.M., W.L., Z.L., M.C., D.X., G.Z., J.W., S.Z., Y.-J.K., D.Z.).|Institut für Biologie und Biotechnologie der Pflanzen, Westfälische Wilhelms-Universität Münster, Schlossplatz 7, 48149 Münster, Germany (J.K.); Department of Oriental Medicinal Biotechnology, College of Life Science, Kyung Hee University, Yongin 446-701, Republic of Korea (Y.-J.K).|Indian Institute of Chemical Biology, Council of Scientific and Industrial Research, 700 032 West Bengal, India (S.B.); and.|School of Agriculture, Food and Wine, University of Adelaide, Waite Campus, Urrbrae, SA 5064, Australia (M.R.T., D.Z.).
Matthew R
0000-0003-4661-6700
MR
Tucker
Joint International Research Laboratory of Metabolic & Developmental Sciences, Shanghai Jiao Tong University-University of Adelaide Joint Centre for Agriculture and Health, School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai 200240, China (J.Y., Z.M., W.L., Z.L., M.C., D.X., G.Z., J.W., S.Z., Y.-J.K., D.Z.).|Institut für Biologie und Biotechnologie der Pflanzen, Westfälische Wilhelms-Universität Münster, Schlossplatz 7, 48149 Münster, Germany (J.K.); Department of Oriental Medicinal Biotechnology, College of Life Science, Kyung Hee University, Yongin 446-701, Republic of Korea (Y.-J.K).|Indian Institute of Chemical Biology, Council of Scientific and Industrial Research, 700 032 West Bengal, India (S.B.); and.|School of Agriculture, Food and Wine, University of Adelaide, Waite Campus, Urrbrae, SA 5064, Australia (M.R.T., D.Z.).
Zhijing
Z
Luo
Joint International Research Laboratory of Metabolic & Developmental Sciences, Shanghai Jiao Tong University-University of Adelaide Joint Centre for Agriculture and Health, School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai 200240, China (J.Y., Z.M., W.L., Z.L., M.C., D.X., G.Z., J.W., S.Z., Y.-J.K., D.Z.).|Institut für Biologie und Biotechnologie der Pflanzen, Westfälische Wilhelms-Universität Münster, Schlossplatz 7, 48149 Münster, Germany (J.K.); Department of Oriental Medicinal Biotechnology, College of Life Science, Kyung Hee University, Yongin 446-701, Republic of Korea (Y.-J.K).|Indian Institute of Chemical Biology, Council of Scientific and Industrial Research, 700 032 West Bengal, India (S.B.); and.|School of Agriculture, Food and Wine, University of Adelaide, Waite Campus, Urrbrae, SA 5064, Australia (M.R.T., D.Z.).
Mingjiao
0000-0002-9079-5980
M
Chen
Joint International Research Laboratory of Metabolic & Developmental Sciences, Shanghai Jiao Tong University-University of Adelaide Joint Centre for Agriculture and Health, School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai 200240, China (J.Y., Z.M., W.L., Z.L., M.C., D.X., G.Z., J.W., S.Z., Y.-J.K., D.Z.).|Institut für Biologie und Biotechnologie der Pflanzen, Westfälische Wilhelms-Universität Münster, Schlossplatz 7, 48149 Münster, Germany (J.K.); Department of Oriental Medicinal Biotechnology, College of Life Science, Kyung Hee University, Yongin 446-701, Republic of Korea (Y.-J.K).|Indian Institute of Chemical Biology, Council of Scientific and Industrial Research, 700 032 West Bengal, India (S.B.); and.|School of Agriculture, Food and Wine, University of Adelaide, Waite Campus, Urrbrae, SA 5064, Australia (M.R.T., D.Z.).
Dawei
0000-0001-8324-450X
D
Xu
Joint International Research Laboratory of Metabolic & Developmental Sciences, Shanghai Jiao Tong University-University of Adelaide Joint Centre for Agriculture and Health, School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai 200240, China (J.Y., Z.M., W.L., Z.L., M.C., D.X., G.Z., J.W., S.Z., Y.-J.K., D.Z.).|Institut für Biologie und Biotechnologie der Pflanzen, Westfälische Wilhelms-Universität Münster, Schlossplatz 7, 48149 Münster, Germany (J.K.); Department of Oriental Medicinal Biotechnology, College of Life Science, Kyung Hee University, Yongin 446-701, Republic of Korea (Y.-J.K).|Indian Institute of Chemical Biology, Council of Scientific and Industrial Research, 700 032 West Bengal, India (S.B.); and.|School of Agriculture, Food and Wine, University of Adelaide, Waite Campus, Urrbrae, SA 5064, Australia (M.R.T., D.Z.).
Guochao
0000-0002-2825-9554
G
Zhao
Joint International Research Laboratory of Metabolic & Developmental Sciences, Shanghai Jiao Tong University-University of Adelaide Joint Centre for Agriculture and Health, School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai 200240, China (J.Y., Z.M., W.L., Z.L., M.C., D.X., G.Z., J.W., S.Z., Y.-J.K., D.Z.).|Institut für Biologie und Biotechnologie der Pflanzen, Westfälische Wilhelms-Universität Münster, Schlossplatz 7, 48149 Münster, Germany (J.K.); Department of Oriental Medicinal Biotechnology, College of Life Science, Kyung Hee University, Yongin 446-701, Republic of Korea (Y.-J.K).|Indian Institute of Chemical Biology, Council of Scientific and Industrial Research, 700 032 West Bengal, India (S.B.); and.|School of Agriculture, Food and Wine, University of Adelaide, Waite Campus, Urrbrae, SA 5064, Australia (M.R.T., D.Z.).
Jie
J
Wang
Joint International Research Laboratory of Metabolic & Developmental Sciences, Shanghai Jiao Tong University-University of Adelaide Joint Centre for Agriculture and Health, School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai 200240, China (J.Y., Z.M., W.L., Z.L., M.C., D.X., G.Z., J.W., S.Z., Y.-J.K., D.Z.).|Institut für Biologie und Biotechnologie der Pflanzen, Westfälische Wilhelms-Universität Münster, Schlossplatz 7, 48149 Münster, Germany (J.K.); Department of Oriental Medicinal Biotechnology, College of Life Science, Kyung Hee University, Yongin 446-701, Republic of Korea (Y.-J.K).|Indian Institute of Chemical Biology, Council of Scientific and Industrial Research, 700 032 West Bengal, India (S.B.); and.|School of Agriculture, Food and Wine, University of Adelaide, Waite Campus, Urrbrae, SA 5064, Australia (M.R.T., D.Z.).
Siyi
S
Zhang
Joint International Research Laboratory of Metabolic & Developmental Sciences, Shanghai Jiao Tong University-University of Adelaide Joint Centre for Agriculture and Health, School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai 200240, China (J.Y., Z.M., W.L., Z.L., M.C., D.X., G.Z., J.W., S.Z., Y.-J.K., D.Z.).|Institut für Biologie und Biotechnologie der Pflanzen, Westfälische Wilhelms-Universität Münster, Schlossplatz 7, 48149 Münster, Germany (J.K.); Department of Oriental Medicinal Biotechnology, College of Life Science, Kyung Hee University, Yongin 446-701, Republic of Korea (Y.-J.K).|Indian Institute of Chemical Biology, Council of Scientific and Industrial Research, 700 032 West Bengal, India (S.B.); and.|School of Agriculture, Food and Wine, University of Adelaide, Waite Campus, Urrbrae, SA 5064, Australia (M.R.T., D.Z.).
Yu-Jin
0000-0003-2562-615X
YJ
Kim
Joint International Research Laboratory of Metabolic & Developmental Sciences, Shanghai Jiao Tong University-University of Adelaide Joint Centre for Agriculture and Health, School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai 200240, China (J.Y., Z.M., W.L., Z.L., M.C., D.X., G.Z., J.W., S.Z., Y.-J.K., D.Z.); zhangdb@sjtu.edu.cn.|Institut für Biologie und Biotechnologie der Pflanzen, Westfälische Wilhelms-Universität Münster, Schlossplatz 7, 48149 Münster, Germany (J.K.); Department of Oriental Medicinal Biotechnology, College of Life Science, Kyung Hee University, Yongin 446-701, Republic of Korea (Y.-J.K); zhangdb@sjtu.edu.cn.|Indian Institute of Chemical Biology, Council of Scientific and Industrial Research, 700 032 West Bengal, India (S.B.); and zhangdb@sjtu.edu.cn.|School of Agriculture, Food and Wine, University of Adelaide, Waite Campus, Urrbrae, SA 5064, Australia (M.R.T., D.Z.) zhangdb@sjtu.edu.cn.
Dabing
0000-0002-1764-2929
D
Zhang
D002135:Calcium-Binding Proteins / Q000378:metabolism*; D016923:Cell Death; D003001:Cloning, Molecular; D053938:DNA Fragmentation; D018506:Gene Expression Regulation, Plant; D006706:Homeostasis; D008954:Models, Biological; D009154:Mutation / Q000235:genetics; D012275:Oryza / Q000033:anatomy & histology* / Q000235:genetics / Q000378:metabolism* / Q000648:ultrastructure; D010641:Phenotype; D010802:Phylogeny; D010940:Plant Proteins / Q000378:metabolism*; D030821:Plants, Genetically Modified; D011058:Pollen / Q000166:cytology / Q000254:growth & development* / Q000378:metabolism* / Q000648:ultrastructure; D011994:Recombinant Proteins / Q000378:metabolism
D002135:Calcium-Binding Proteins; D010940:Plant Proteins; D011994:Recombinant Proteins; C085577:Ca2+-binding protein-1
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