Convergent selection of a WD40 protein that enhances grain yield in maize and rice

第一作者：WENKANG CHEN

第一单位：中国农业大学

通讯作者：XIAOHONG YANG

 Abstarct 

背景回顾：During the independent process of cereal evolution, many trait shifts appear to have been under convergent selection to meet the specific needs of humans. Identification of convergently selected genes across cereals could help to clarify the evolution of crop species and to accelerate breeding programs. In the past several decades, researchers have debated whether convergent phenotypic selection in distinct lineages is driven by conserved molecular changes or by diverse molecular pathways. Two of the most economically important crops, maize and rice, display some conserved phenotypic shifts—including loss of seed dispersal, decreased seed dormancy, and increased grain number during evolution—even though they experienced independent selection. Hence, maize and rice can serve as an excellent system for understanding the extent of convergent selection among cereals.

在谷类作物独立演化过程中，许多性状的改变显然经历了趋同选择以满足人类的需求。鉴定不同谷类作物中受到趋同选择的基因有助于阐明作物的演化，并且加速作物育种进程。在过去数个世纪里，研究人员一直在争论，不同谱系中的趋同表型选择是否受到保守的分子改变所驱动，还是由不同的分子通路所驱动？玉米和水稻是两种最好的经济作物，尽管这两个物种经历了独立的选择，但是在落粒性丢失、种子休眠减少以及籽粒数量增加等性状上存在明显的趋同表型变化。因此，玉米和水稻可以作为一个比较理想的平台，用以研究不同谷类作物之间的趋同选择。

研究基础：Despite the identification of a few convergently selected genes, our understanding of the extent of molecular convergence on a genome-wide scale between maize and rice is very limited. To learn how often selection acts on orthologous genes, we investigated the functions and molecular evolution of the grain yield quantitative trait locus KRN2 in maize and its rice ortholog OsKRN2. We also identified convergently selected genes on a genome-wide scale in maize and rice, using two large datasets. 

尽管目前已经鉴定了一些受到趋同选择的基因，但是我们对于水稻和玉米在全基因组尺度上的分子趋同程度还不清楚。为了进一步了解选择作用于直系同源基因的频率，作者研究了玉米中籽粒产量数量性状位点KRN2及其在水稻中的直接同源基因OsKRN2的功能和分子演化。作者还通过两个大的数据集，从全基因组水平鉴定了玉米和水稻中受到趋同选择的基因。

结果1-KRN2/OsKRN2：We identified a selected gene, KRN2 (kernel row number2), that differs between domesticated maize and its wild ancestor, teosinte. This gene underlies a major quantitative trait locus for kernel row number in maize. Selection in the noncoding upstream regions resulted in a reduction of KRN2 expression and an increased grain number through an increase in kernel rows. The rice ortholog, OsKRN2, also underwent selection and negatively regulates grain number via control of secondary panicle branches. These orthologs encode WD40 proteins and function synergistically with a gene of unknown function, DUF1644, which suggests that a conserved protein interaction controls grain number in maize and rice. Field tests show that knockout of KRN2 in maize or OsKRN2 in rice increased grain yield by ~10% and ~8%, respectively, with no apparent trade-off in other agronomic traits. This suggests potential applications of KRN2 and its orthologs for crop improvement.

作者鉴定到了一个受到选择的基因KRN2在驯化玉米及其祖先野生种大刍草中存在差异。该基因是玉米穗行数的主效数量性状位点。对于KRN2基因上游非编码区的选择导致了KRN2基因的表达量下降，导致了穗行数的增加，最终导致了玉米籽粒量增加。水稻中的直系同源基因OsKRN2同样经历了选择，并且通过控制次生穗分枝负调控籽粒量。这些直系同源基因编码一个WD40蛋白，且均能够与一个功能未知基因DUF1644协同作用，表明玉米和水稻中WD40蛋白存在保守的蛋白互作效应作用于籽粒产量。田间试验显示玉米KRN2和水稻OsKRN2的敲除能够分别增加约10%和8%的产量，同时对于其他农艺性状不存在明显负面影响。这表明KRN2及其直系同源基因在作物育种改良中具有潜在应用价值。

结果2-全基因组水平上的趋同选择基因：On a genome-wide scale, we identified a set of 490 orthologous genes that underwent convergent selection during maize and rice evolution, including KRN2/OsKRN2. We found that the convergently selected orthologous genes appear to be significantly enriched in two specific pathways in both maize and rice: starch and sucrose metabolism, and biosynthesis of cofactors. A deep analysis of convergently selected genes in the starch metabolic pathway indicates that the degree of genetic convergence via convergent selection is related to the conservation and complexity of the gene network for a given selection.

在全基因组尺度上，作者鉴定到490对玉米和水稻的直系同源基因经历了趋同选择，其中就包括了KRN2/OsKRN2。作者发现受到趋同选择的直系同源基因在玉米和水稻中都显著富集于两个特定的通路：淀粉和蔗糖代谢、辅因子生物合成。通过对受到趋同选择基因在淀粉代谢通路上的深入分析，作者发现趋同选择的遗传趋同程度与基因网络的保守性和复杂度有关。

结论：Our findings show that common phenotypic shifts during maize and rice evolution acting on conserved genes are driven at least in part by convergent selection, which in maize and rice likely occurred both during and after domestication. We provide evolutionary and functional evidence on the convergent selection of KRN2/OsKRN2 for grain number between maize and rice. We further found that a complete loss-of-function allele of KRN2/OsKRN2 increased grain yield without an apparent negative impact on other agronomic traits. Exploring the role of KRN2/OsKRN2 and other convergently selected genes across the cereals could provide new opportunities to enhance the production of other global crops. 

本文的研究显示在玉米和水稻的演化过程中，由保守基因作用的相同表型改变至少部分是由趋同选择所驱动的，而在玉米和水稻中这一过程发生于驯化中和驯化后。作者的研究表明玉米和水稻的KRN2-OsKRN2直系同源基因对的趋同选择作用于籽粒产量。进一步的研究显示，KRN2/OsKRN2的功能缺失能够在不影响其他农艺性状情况下，显著提升籽粒产量。通过对KRN2/OsKRN2以及其他受到趋同选择的基因的深度挖掘，将有助于为未来全球作物的增产提供新的机遇。

** 杨小红 **

doi: https://doi.org/10.1126/science.abg7985

Journal: Science​

Published date:  March 25, 2022