Sporophytic control of tapetal development and pollen fertility by a mitogen-activated protein kinase cascade in rice

被引:7
作者
Zeng, Jianguo [1 ]
Duan, Manman [1 ]
Wang, Yiqing [1 ]
Li, Guangtao [1 ]
You, Yujing [1 ]
Shi, Jie [1 ]
Liu, Changhao [1 ]
Zhang, Jinyang [1 ]
Xu, Juan [2 ]
Zhang, Shuqun [3 ]
Zhao, Jing [1 ]
机构
[1] Nanjing Agr Univ, Dept Plant Pathol, Nanjing 210095, Peoples R China
[2] Zhejiang Univ, Coll Life Sci, State Key Lab Plant Physiol & Biochem, Hangzhou 310058, Peoples R China
[3] Univ Missouri, Div Biochem, Columbia, MO 65211 USA
基金
中国国家自然科学基金;
关键词
degradation; MAPK cascade; pollen fertility; rice; tapetum; ROOT-SYSTEM ARCHITECTURE; WATER-USE EFFICIENCY; TRANSCRIPTION FACTOR; DROUGHT TOLERANCE; PHOSPHATE-STARVATION; YIELD; ASSOCIATION; TRAITS; STRESS; MAIZE;
D O I
10.1111/jipb.13673
中图分类号
Q5 [生物化学]; Q7 [分子生物学];
学科分类号
071010 ; 081704 ;
摘要
Tapetum, the innermost layer of the anther wall, provides essential nutrients and materials for pollen development. Timely degradation of anther tapetal cells is a prerequisite for normal pollen development in flowering plants. Tapetal cells facilitate male gametogenesis by providing cellular contents after highly coordinated programmed cell death (PCD). Tapetal development is regulated by a transcriptional network. However, the signaling pathway(s) involved in this process are poorly understood. In this study, we report that a mitogen-activated protein kinase (MAPK) cascade composed of OsYDA1/OsYDA2-OsMKK4-OsMPK6 plays an important role in tapetal development and male gametophyte fertility. Loss of function of this MAPK cascade leads to anther indehiscence, enlarged tapetum, and aborted pollen grains. Tapetal cells in osmkk4 and osmpk6 mutants exhibit an increased presence of lipid body-like structures within the cytoplasm, which is accompanied by a delayed occurrence of PCD. Expression of a constitutively active version of OsMPK6 (CA-OsMPK6) can rescue the pollen defects in osmkk4 mutants, confirming that OsMPK6 functions downstream of OsMKK4 in this pathway. Genetic crosses also demonstrated that the MAPK cascade sporophyticly regulates pollen development. Our study reveals a novel function of rice MAPK cascade in plant male reproductive biology. A mitogen-activated protein kinase (MAPK) cascade composed of OsYDA1/OsYDA2-OsMKK4-OsMPK6 plays an important role in tapetal development and male gametophyte fertility. Loss of function of this MAPK cascade leads to anther indehiscence, enlarged tapetum, and aborted pollen grains. This study reveals a novel function of rice MAPK cascade in plant male reproductive biology. image
引用
收藏
页码:1500 / 1516
页数:17
相关论文
共 61 条
[1]   Genetic Regulation of Sporopollenin Synthesis and Pollen Exine Development [J].
Ariizumi, Tohru ;
Toriyama, Kinya .
ANNUAL REVIEW OF PLANT BIOLOGY, VOL 62, 2011, 62 :437-460
[2]   Paternal Control of Embryonic Patterning in Arabidopsis thaliana [J].
Bayer, Martin ;
Nawy, Tal ;
Giglione, Carmela ;
Galli, Mary ;
Meinnel, Thierry ;
Lukowitz, Wolfgang .
SCIENCE, 2009, 323 (5920) :1485-1488
[3]   Stomatal development and pattern controlled by a MAPKK kinase [J].
Bergmann, DC ;
Lukowitz, W ;
Somerville, CR .
SCIENCE, 2004, 304 (5676) :1494-1497
[4]   Constitutively Active Mitogen-Activated Protein Kinase Versions Reveal Functions of Arabidopsis MPK4 in Pathogen Defense Signaling [J].
Berriri, Souha ;
Garcia, Ana Victoria ;
Frey, Nicolas Frei Dit ;
Rozhon, Wilfried ;
Pateyron, Stephanie ;
Leonhardt, Nathalie ;
Montillet, Jean-Luc ;
Leung, Jeffrey ;
Hirt, Heribert ;
Colcombet, Jean .
PLANT CELL, 2012, 24 (10) :4281-4293
[5]   Mutational evidence that the Arabidopsis MAP kinase MPK6 is involved in anther, inflorescence, and embryo development [J].
Bush, Susan M. ;
Krysan, Patrick J. .
JOURNAL OF EXPERIMENTAL BOTANY, 2007, 58 (08) :2181-2191
[6]   BES1 is activated by EMS1-TPD1-SERK1/2-mediated signaling to control tapetum development in Arabidopsis thaliana [J].
Chen, Weiyue ;
Lv, Minghui ;
Wang, Yanze ;
Wang, Ping-An ;
Cui, Yanwei ;
Li, Meizhen ;
Wang, Ruoshi ;
Gou, Xiaoping ;
Li, Jia .
NATURE COMMUNICATIONS, 2019, 10 (1)
[7]   Arabidopsis SOMATIC EMBRYOGENESIS RECEPTOR KINASES1 and 2 are essential for tapetum development and microspore maturation [J].
Colcombet, J ;
Boisson-Dernier, A ;
Ros-Palau, R ;
Vera, CE ;
Schroeder, JI .
PLANT CELL, 2005, 17 (12) :3350-3361
[8]   SMALL GRAIN 1, which encodes a mitogen-activated protein kinase kinase 4, influences grain size in rice [J].
Duan, Penggen ;
Rao, Yuchun ;
Zeng, Dali ;
Yang, Yaolong ;
Xu, Ran ;
Zhang, Baolan ;
Dong, Guojun ;
Qian, Qian ;
Li, Yunhai .
PLANT JOURNAL, 2014, 77 (04) :547-557
[9]   Efficient genome editing in plants using a CRISPR/Cas system [J].
Feng, Zhengyan ;
Zhang, Botao ;
Ding, Wona ;
Liu, Xiaodong ;
Yang, Dong-Lei ;
Wei, Pengliang ;
Cao, Fengqiu ;
Zhu, Shihua ;
Zhang, Feng ;
Mao, Yanfei ;
Zhu, Jian-Kang .
CELL RESEARCH, 2013, 23 (10) :1229-1232
[10]   The Rice Basic Helix-Loop-Helix Transcription Factor TDR INTERACTING PROTEIN2 Is a Central Switch in Early Anther Development [J].
Fu, Zhenzhen ;
Yu, Jing ;
Cheng, Xiaowei ;
Zong, Xu ;
Xu, Jie ;
Chen, Mingjiao ;
Li, Zongyun ;
Zhang, Dabing ;
Liang, Wanqi .
PLANT CELL, 2014, 26 (04) :1512-1524