The New Is Old: Novel Germination Strategy Evolved From Standing Genetic Variation in Weedy Rice

Feralization of crop plants has aroused an increasing interest in recent years, not only for the reduced yield and quality of crop production caused by feral plants but also for the rapid evolution of novel traits that facilitate the evolution and persistence of weedy forms. Weedy rice (Oryza sativa...

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Main Authors: Chengchuan Zhou, Yang Feng, Gengyun Li, Mengli Wang, Jinjing Jian, Yuguo Wang, Wenju Zhang, Zhiping Song, Linfeng Li, Baorong Lu, Ji Yang
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-06-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2021.699464/full
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author Chengchuan Zhou
Yang Feng
Gengyun Li
Mengli Wang
Jinjing Jian
Yuguo Wang
Wenju Zhang
Zhiping Song
Linfeng Li
Baorong Lu
Ji Yang
Ji Yang
author_facet Chengchuan Zhou
Yang Feng
Gengyun Li
Mengli Wang
Jinjing Jian
Yuguo Wang
Wenju Zhang
Zhiping Song
Linfeng Li
Baorong Lu
Ji Yang
Ji Yang
author_sort Chengchuan Zhou
collection DOAJ
description Feralization of crop plants has aroused an increasing interest in recent years, not only for the reduced yield and quality of crop production caused by feral plants but also for the rapid evolution of novel traits that facilitate the evolution and persistence of weedy forms. Weedy rice (Oryza sativa f. spontanea) is a conspecific weed of cultivated rice, with separate and independent origins. The weedy rice distributed in eastern and northeastern China did not diverge from their cultivated ancestors by reverting to the pre-domestication trait of seed dormancy during feralization. Instead, they developed a temperature-sensing mechanism to control the timing of seed germination. Subsequent divergence in the minimum critical temperature for germination has been detected between northeastern and eastern populations. An integrative analysis was conducted using combinations of phenotypic, genomic and transcriptomic data to investigate the genetic mechanism underlying local adaptation and feralization. A dozen genes were identified, which showed extreme allele frequency differences between eastern and northeastern populations, and high correlations between allele-specific gene expression and feral phenotypes. Trancing the origin of potential adaptive alleles based on genomic sequences revealed the presence of most selected alleles in wild and cultivated rice genomes, indicating that weedy rice drew upon pre-existing, “conditionally neutral” alleles to respond to the feral selection regimes. The cryptic phenotype was exposed by activating formerly silent alleles to facilitate the transition from cultivation to wild existence, promoting the evolution and persistence of weedy forms.
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spelling doaj.art-2bb26ccadeff492b9a223bd8269ae6142022-12-21T22:05:23ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2021-06-011210.3389/fpls.2021.699464699464The New Is Old: Novel Germination Strategy Evolved From Standing Genetic Variation in Weedy RiceChengchuan Zhou0Yang Feng1Gengyun Li2Mengli Wang3Jinjing Jian4Yuguo Wang5Wenju Zhang6Zhiping Song7Linfeng Li8Baorong Lu9Ji Yang10Ji Yang11National Observations and Research Station for Wetland Ecosystems of the Yangtze Estuary, Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, Fudan University, Shanghai, ChinaNational Observations and Research Station for Wetland Ecosystems of the Yangtze Estuary, Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, Fudan University, Shanghai, ChinaNational Observations and Research Station for Wetland Ecosystems of the Yangtze Estuary, Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, Fudan University, Shanghai, ChinaNational Observations and Research Station for Wetland Ecosystems of the Yangtze Estuary, Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, Fudan University, Shanghai, ChinaNational Observations and Research Station for Wetland Ecosystems of the Yangtze Estuary, Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, Fudan University, Shanghai, ChinaNational Observations and Research Station for Wetland Ecosystems of the Yangtze Estuary, Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, Fudan University, Shanghai, ChinaNational Observations and Research Station for Wetland Ecosystems of the Yangtze Estuary, Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, Fudan University, Shanghai, ChinaNational Observations and Research Station for Wetland Ecosystems of the Yangtze Estuary, Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, Fudan University, Shanghai, ChinaNational Observations and Research Station for Wetland Ecosystems of the Yangtze Estuary, Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, Fudan University, Shanghai, ChinaNational Observations and Research Station for Wetland Ecosystems of the Yangtze Estuary, Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, Fudan University, Shanghai, ChinaNational Observations and Research Station for Wetland Ecosystems of the Yangtze Estuary, Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, Fudan University, Shanghai, ChinaShanghai Key Laboratory of Plant Functional Genomics and Resources, Shanghai Chenshan Botanical Garden, Shanghai, ChinaFeralization of crop plants has aroused an increasing interest in recent years, not only for the reduced yield and quality of crop production caused by feral plants but also for the rapid evolution of novel traits that facilitate the evolution and persistence of weedy forms. Weedy rice (Oryza sativa f. spontanea) is a conspecific weed of cultivated rice, with separate and independent origins. The weedy rice distributed in eastern and northeastern China did not diverge from their cultivated ancestors by reverting to the pre-domestication trait of seed dormancy during feralization. Instead, they developed a temperature-sensing mechanism to control the timing of seed germination. Subsequent divergence in the minimum critical temperature for germination has been detected between northeastern and eastern populations. An integrative analysis was conducted using combinations of phenotypic, genomic and transcriptomic data to investigate the genetic mechanism underlying local adaptation and feralization. A dozen genes were identified, which showed extreme allele frequency differences between eastern and northeastern populations, and high correlations between allele-specific gene expression and feral phenotypes. Trancing the origin of potential adaptive alleles based on genomic sequences revealed the presence of most selected alleles in wild and cultivated rice genomes, indicating that weedy rice drew upon pre-existing, “conditionally neutral” alleles to respond to the feral selection regimes. The cryptic phenotype was exposed by activating formerly silent alleles to facilitate the transition from cultivation to wild existence, promoting the evolution and persistence of weedy forms.https://www.frontiersin.org/articles/10.3389/fpls.2021.699464/fullweedy ricecrop feralizationgermination strategyrapid adaptationstanding genetic variation
spellingShingle Chengchuan Zhou
Yang Feng
Gengyun Li
Mengli Wang
Jinjing Jian
Yuguo Wang
Wenju Zhang
Zhiping Song
Linfeng Li
Baorong Lu
Ji Yang
Ji Yang
The New Is Old: Novel Germination Strategy Evolved From Standing Genetic Variation in Weedy Rice
Frontiers in Plant Science
weedy rice
crop feralization
germination strategy
rapid adaptation
standing genetic variation
title The New Is Old: Novel Germination Strategy Evolved From Standing Genetic Variation in Weedy Rice
title_full The New Is Old: Novel Germination Strategy Evolved From Standing Genetic Variation in Weedy Rice
title_fullStr The New Is Old: Novel Germination Strategy Evolved From Standing Genetic Variation in Weedy Rice
title_full_unstemmed The New Is Old: Novel Germination Strategy Evolved From Standing Genetic Variation in Weedy Rice
title_short The New Is Old: Novel Germination Strategy Evolved From Standing Genetic Variation in Weedy Rice
title_sort new is old novel germination strategy evolved from standing genetic variation in weedy rice
topic weedy rice
crop feralization
germination strategy
rapid adaptation
standing genetic variation
url https://www.frontiersin.org/articles/10.3389/fpls.2021.699464/full
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