FERONIA receptor kinase-regulated reactive oxygen species mediate self-incompatibility in Brassica rapa

被引:84
作者
Zhang, Lili [1 ,2 ]
Huang, Jiabao [1 ,2 ]
Su, Shiqi [1 ,2 ]
Wei, Xiaochun [4 ]
Yang, Lin [1 ,2 ]
Zhao, Huanhuan [1 ,2 ]
Yu, Jianqiang [1 ,2 ]
Wang, Jie [1 ,2 ]
Hui, Jiyun [1 ,2 ]
Hao, Shiya [3 ]
Song, Shanshan [1 ,2 ]
Cao, Yanyan [1 ,2 ]
Wang, Maoshuai [1 ,2 ]
Zhang, Xiaowei [4 ]
Zhao, Yanyan [4 ]
Wang, Zhiyong [4 ]
Zeng, Weiqing [6 ,7 ]
Wu, Hen-Ming [5 ]
Yuan, Yuxiang [4 ]
Zhang, Xiansheng [1 ]
Cheung, Alice Y. [5 ]
Duan, Qiaohong [1 ,2 ]
机构
[1] Shandong Agr Univ, State Key Lab Crop Biol, Tai An 271018, Shandong, Peoples R China
[2] Shandong Agr Univ, China Coll Hort Sci & Engn, Tai An 271018, Shandong, Peoples R China
[3] Rutgers State Univ, Sch Arts & Sci, New Brunswick, NJ 08901 USA
[4] Henan Acad Agr Sci, Inst Hort, Zhengzhou 450002, Henan, Peoples R China
[5] Univ Massachusetts, Dept Biochem & Mol Biol, Mol Cell Biol & Plant Biol Programs, Amherst, NY 01003 USA
[6] 9220 Enfield Dr, Johnston, IA 50131 USA
[7] Corteva Agrisci, Trait Discovery, Johnston, IA 50131 USA
基金
美国国家科学基金会;
关键词
PROGRAMMED CELL-DEATH; E3 LIGASE PROMOTES; NADPH OXIDASE; ARABIDOPSIS-THALIANA; HYDROGEN-PEROXIDE; PLASMA-MEMBRANE; POLLEN; ARC1; GENE; BINDING;
D O I
10.1016/j.cub.2021.04.060
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
Most plants in the Brassicaceae evolve self-incompatibility (SI) to avoid inbreeding and generate hybrid vigor. Self-pollen is recognized by the S-haplotype-specific interaction of the pollen ligand S-locus protein 11 (SP11) (also known as S-locus cysteine-rich protein [SCR]) and its stigma-specific S-locus receptor kinase (SRK). However, mechanistically much remains unknown about the signaling events that culminate in self pollen rejection. Here, we show that self-pollen triggers high levels of reactive oxygen species (ROS) in stigma papilla cells to mediate SI in heading Chinese cabbage (Brassica rapa L. ssp. pekinensis). We found that stigmatic ROS increased after self-pollination but decreased after compatible(CP)-pollination. Reducing stigmatic ROS by scavengers or suppressing the expression of respiratory burst oxidase homologs (Rbohs), which encode plant NADPH oxidases that produce ROS, both broke down SI. On the other hand, increasing the level of ROS inhibited the germination and penetration of compatible pollen on the stigma, mimicking an incompatible response. Furthermore, suppressing a B. rapa FERONIA (FER) receptor kinase homolog or Rac/ Rop guanosine triphosphatase (GTPase) signaling effectively reduced stigmatic ROS and interfered with SI. Our results suggest that FER-Rac/Rop signaling-regulated, NADPH oxidase-produced ROS is an essential SI response leading to self-pollen rejection.
引用
收藏
页码:3004 / U72
页数:18
相关论文
共 100 条
  • [1] Genome-wide Insertional mutagenesis of Arabidopsis thaliana
    Alonso, JM
    Stepanova, AN
    Leisse, TJ
    Kim, CJ
    Chen, HM
    Shinn, P
    Stevenson, DK
    Zimmerman, J
    Barajas, P
    Cheuk, R
    Gadrinab, C
    Heller, C
    Jeske, A
    Koesema, E
    Meyers, CC
    Parker, H
    Prednis, L
    Ansari, Y
    Choy, N
    Deen, H
    Geralt, M
    Hazari, N
    Hom, E
    Karnes, M
    Mulholland, C
    Ndubaku, R
    Schmidt, I
    Guzman, P
    Aguilar-Henonin, L
    Schmid, M
    Weigel, D
    Carter, DE
    Marchand, T
    Risseeuw, E
    Brogden, D
    Zeko, A
    Crosby, WL
    Berry, CC
    Ecker, JR
    [J]. SCIENCE, 2003, 301 (5633) : 653 - 657
  • [2] The transition to self-compatibility in Arabidopsis thaliana and evolution within S-haplotypes over 10 Myr
    Bechsgaard, Jesper S.
    Castric, Vincent
    Charlesworth, Deborah
    Vekemans, Xavier
    Schierup, Mikkel H.
    [J]. MOLECULAR BIOLOGY AND EVOLUTION, 2006, 23 (09) : 1741 - 1750
  • [3] Pollen-Pistil Interactions and Their Role in Mate Selection
    Bedinger, Patricia A.
    Broz, Amanda K.
    Tovar-Mendez, Alejandro
    McClure, Bruce
    [J]. PLANT PHYSIOLOGY, 2017, 173 (01) : 79 - 90
  • [4] Bezvoda R, 2014, METHODS MOL BIOL, V1080, P231, DOI 10.1007/978-1-62703-643-6_19
  • [5] Independent S-Locus Mutations Caused Self-Fertility in Arabidopsis thaliana
    Boggs, Nathan A.
    Nasrallah, June B.
    Nasrallah, Mikhail E.
    [J]. PLOS GENETICS, 2009, 5 (03):
  • [6] ANXUR Receptor-Like Kinases Coordinate Cell Wall Integrity with Growth at the Pollen Tube Tip Via NADPH Oxidases
    Boisson-Dernier, Aurelien
    Lituiev, Dmytro S.
    Nestorova, Anna
    Franck, Christina Maria
    Thirugnanarajah, Sharme
    Grossniklaus, Ueli
    [J]. PLOS BIOLOGY, 2013, 11 (11)
  • [7] Pollen-stigma interactions in Brassicaceae: complex communication events regulating pollen hydration
    Bosch, Maurice
    Wang, Ludi
    [J]. JOURNAL OF EXPERIMENTAL BOTANY, 2020, 71 (09) : 2465 - 2468
  • [8] Initiation of Programmed Cell Death in Self-incompatibility: Role for Cytoskeleton Modifications and Several Caspase-Like Activities
    Bosch, Maurice
    Poulter, Natalie S.
    Vatovec, Sabina
    Franklin-Tong, Vernonica E.
    [J]. MOLECULAR PLANT, 2008, 1 (06) : 879 - 887
  • [9] ABA-induced NO generation and stomatal closure in Arabidopsis are dependent on H2O2 synthesis
    Bright, J
    Desikan, R
    Hancock, JT
    Weir, IS
    Neill, SJ
    [J]. PLANT JOURNAL, 2006, 45 (01) : 113 - 122
  • [10] Brassica rapa Genome 2.0: A Reference Upgrade through Sequence Re-assembly and Gene Re-annotation
    Cai, Chengcheng
    Wang, Xiaobo
    Liu, Bo
    Wu, Jian
    Liang, Jianli
    Cui, Yinan
    Cheng, Feng
    Wang, Xiaowu
    [J]. MOLECULAR PLANT, 2017, 10 (04) : 649 - 651