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Cysteine-rich peptides promote interspecific genetic isolation in Arabidopsis.

ABSTRACT: Reproductive isolation is a prerequisite for speciation. Failure of communication between female tissues of the pistil and paternal pollen tubes imposes hybridization barriers in flowering plants. Arabidopsis thaliana LURE1 (AtLURE1) peptides and their male receptor PRK6 aid attraction of the growing pollen tube to the ovule. Here, we report that the knockout of the entire AtLURE1 gene family did not affect fertility, indicating that AtLURE1-PRK6-mediated signaling is not required for successful fertilization within one Arabidopsis species. AtLURE1s instead function as pollen tube emergence accelerators that favor conspecific pollen over pollen from other species and thus promote reproductive isolation. We also identified maternal peptides XIUQIU1 to -4, which attract pollen tubes regardless of species. Cooperation between ovule attraction and pollen tube growth acceleration favors conspecific fertilization and promotes reproductive isolation.

SUBMITTER: Zhong S

PROVIDER: S-EPMC7184628 | biostudies-literature | 2019 May

REPOSITORIES: biostudies-literature

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Cysteine-rich peptides promote interspecific genetic isolation in Arabidopsis.

Zhong Sheng S Liu Meiling M Wang Zhijuan Z Huang Qingpei Q Hou Saiying S Xu Yong-Chao YC Ge Zengxiang Z Song Zihan Z Huang Jiaying J Qiu Xinyu X Shi Yihao Y Xiao Junyu J Liu Pei P Guo Ya-Long YL Dong Juan J Dresselhaus Thomas T Gu Hongya H Qu Li-Jia LJ

Science (New York, N.Y.) 20190501 6443

Reproductive isolation is a prerequisite for speciation. Failure of communication between female tissues of the pistil and paternal pollen tubes imposes hybridization barriers in flowering plants. Arabidopsis thaliana LURE1 (AtLURE1) peptides and their male receptor PRK6 aid attraction of the growing pollen tube to the ovule. Here, we report that the knockout of the entire AtLURE1 gene family did not affect fertility, indicating that AtLURE1-PRK6-mediated signaling is not required ...[more]

PMID: 31147494

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Project description:BACKGROUND: In plants, transposons and non-protein-coding repeats are epigenetically silenced by CG and non-CG methylation. This pattern of methylation is mediated in part by small RNAs and two specialized RNA polymerases, termed Pol IV and Pol V, in a process called RNA-directed DNA methylation. By contrast, many protein-coding genes transcribed by Pol II contain in their gene bodies exclusively CG methylation that is independent of small RNAs and Pol IV/Pol V activities. It is unclear how the different methylation machineries distinguish between transposons and genes. Here we report on a group of atypical genes that display in their coding region a transposon-like methylation pattern, which is associated with gene silencing in sporophytic tissues. RESULTS: We performed a methylation-sensitive amplification polymorphism analysis to search for targets of RNA-directed DNA methylation in Arabidopsis thaliana and identified several members of a gene family encoding cysteine-rich peptides (CRPs). In leaves, the CRP genes are silent and their coding regions contain dense, transposon-like methylation in CG, CHG and CHH contexts, which depends partly on the Pol IV/Pol V pathway and small RNAs. Methylation in the coding region is reduced, however, in the synergid cells of the female gametophyte, where the CRP genes are specifically expressed. Further demonstrating that expressed CRP genes lack gene body methylation, a CRP4-GFP fusion gene under the control of the constitutive 35?S promoter remains unmethylated in leaves and is transcribed to produce a translatable mRNA. By contrast, a CRP4-GFP fusion gene under the control of a CRP4 promoter fragment acquires CG and non-CG methylation in the CRP coding region in leaves similar to the silent endogenous CRP4 gene. CONCLUSIONS: Unlike CG methylation in gene bodies, which does not dramatically affect Pol II transcription, combined CG and non-CG methylation in CRP coding regions is likely to contribute to gene silencing in leaves because loss of this methylation in synergid cells is associated with CRP gene expression. We discuss this unusual methylation pattern and its alteration in synergid cells as well as the possible retrogene origin and evolutionary significance of CRP genes that are methylated like transposons.

Dataset Information

Cysteine-rich peptides promote interspecific genetic isolation in Arabidopsis.

Publications

Cysteine-rich peptides promote interspecific genetic isolation in <i>Arabidopsis</i>.

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