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Stigma receptors control intraspecies and interspecies barriers in Brassicaceae.

ABSTRACT: Flowering plants have evolved numerous intraspecific and interspecific prezygotic reproductive barriers to prevent production of unfavourable offspring¹. Within a species, self-incompatibility (SI) is a widely utilized mechanism that rejects self-pollen^2,3 to avoid inbreeding depression. Interspecific barriers restrain breeding between species and often follow the SI × self-compatible (SC) rule, that is, interspecific pollen is unilaterally incompatible (UI) on SI pistils but unilaterally compatible (UC) on SC pistils^1,4-6. The molecular mechanisms underlying SI, UI, SC and UC and their interconnections in the Brassicaceae remain unclear. Here we demonstrate that the SI pollen determinant S-locus cysteine-rich protein/S-locus protein 11 (SCR/SP11)^2,3 or a signal from UI pollen binds to the SI female determinant S-locus receptor kinase (SRK)^2,3, recruits FERONIA (FER)^7-9 and activates FER-mediated reactive oxygen species production in SI stigmas^10,11 to reject incompatible pollen. For compatible responses, diverged pollen coat protein B-class^12-14 from SC and UC pollen differentially trigger nitric oxide, nitrosate FER to suppress reactive oxygen species in SC stigmas to facilitate pollen growth in an intraspecies-preferential manner, maintaining species integrity. Our results show that SRK and FER integrate mechanisms underlying intraspecific and interspecific barriers and offer paths to achieve distant breeding in Brassicaceae crops.

SUBMITTER: Huang J

PROVIDER: S-EPMC9908550 | biostudies-literature | 2023 Feb

REPOSITORIES: biostudies-literature

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Stigma receptors control intraspecies and interspecies barriers in Brassicaceae.

Huang Jiabao J Yang Lin L Yang Liu L Wu Xiaoyu X Cui Xiaoshuang X Zhang Lili L Hui Jiyun J Zhao Yumei Y Yang Hongmin H Liu Shangjia S Xu Quanling Q Pang Maoxuan M Guo Xinping X Cao Yunyun Y Chen Yu Y Ren Xinru X Lv Jinzhi J Yu Jianqiang J Ding Junyi J Xu Gang G Wang Nian N Wei Xiaochun X Lin Qinghui Q Yuan Yuxiang Y Zhang Xiaowei X Ma Chaozhi C Dai Cheng C Wang Pengwei P Wang Yongchao Y Cheng Fei F Zeng Weiqing W Palanivelu Ravishankar R Wu Hen-Ming HM Zhang Xiansheng X Cheung Alice Y AY Duan Qiaohong Q

Nature 20230125 7947

Flowering plants have evolved numerous intraspecific and interspecific prezygotic reproductive barriers to prevent production of unfavourable offspring<sup>1</sup>. Within a species, self-incompatibility (SI) is a widely utilized mechanism that rejects self-pollen<sup>2,3</sup> to avoid inbreeding depression. Interspecific barriers restrain breeding between species and often follow the SI × self-compatible (SC) rule, that is, interspecific pollen is unilaterally incompatible (UI) on SI pistils b ...[more]

PMID: 36697825

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Project description:The twitching motility of bacteria is closely related to environmental adaptability and pathogenic behaviors. Lysobacter is a good genus in which to study twitching motility because of the complex social activities and distinct movement patterns of its members. Regardless, the mechanism that induces twitching motility is largely unknown. In this study, we found that the interspecies signal indole caused Lysobacter to have irregular, random twitching motility with significantly enhanced speed. Deletion of qseC or qseB from the two-component system for indole signaling perception resulted in the disappearance of rapid, random movements and significantly decreased twitching activity. Indole-induced, rapid, random twitching was achieved through upregulation of expression of gene cluster pilE1-pilY11-pilX1-pilW1-pilV1-fimT1 In addition, under conditions of extremely low bacterial density, individual Lysobacter cells grew and divided in a stable manner in situ without any movement. The intraspecies quorum-sensing signaling factor 13-methyltetradecanoic acid, designated L. enzymogenes diffusible signaling factor (LeDSF), was essential for Lysobacter to produce twitching motility through indirect regulation of gene clusters pilM-pilN-pilO-pilP-pilQ and pilS1-pilR-pilA-pilB-pilC These results demonstrate that the motility of Lysobacter is induced and regulated by indole and LeDSF, which reveals a novel theory for future studies of the mechanisms of bacterial twitching activities.IMPORTANCE The mechanism underlying bacterial twitching motility is an important research area because it is closely related to social and pathogenic behaviors. The mechanism mediating cell-to-cell perception of twitching motility is largely unknown. Using Lysobacter as a model, we found in this study that the interspecies signal indole caused Lysobacter to exhibit irregular, random twitching motility via activation of gene cluster pilE1-pilY11-pilX1-pilW1-pilV1-fimT1 In addition, population-dependent behavior induced by 13-methyltetradecanoic acid, a quorum-sensing signaling molecule designated LeDSF, was involved in twitching motility by indirectly regulating gene clusters pilM-pilN-pilO-pilP-pilQ and pilS1-pilR-pilA-pilB-pilC The results demonstrate that the twitching motility of Lysobacter is regulated by these two signaling molecules, offering novel clues for exploring the mechanisms of twitching motility and population-dependent behaviors of bacteria.

Dataset Information

Stigma receptors control intraspecies and interspecies barriers in Brassicaceae.

Publications

Stigma receptors control intraspecies and interspecies barriers in Brassicaceae.

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