地區適應演化的關鍵：全基因體關聯分析揭示紅豆開花時間的遺傳結構

Abstract

紅豆（Vigna angularis [Willd.] Ohwi and Ohashi，2n = 22）是東亞及南亞地區的重要豆科作物，其農業與文化價值不可忽視。相較於野生型紅豆（V. angularis var. nipponensis），現今的栽培品系已經拓展至中國北方與日本北海道等高緯度地區。作為短日照植物，紅豆對光週期十分敏感，在短日照條件下促進開花，而在長日照環境中則開花延遲。為能在夏季長日照下完成開花與結實、避免冬季低溫所致的損失，栽培紅豆必須演化出對光週期反應較低的特性。然而，開花時間作為能影響適應性與產量的重要性狀，其在紅豆中的遺傳機制仍未明朗。本研究針對來自東亞及南亞地區的454個地方品系與野生紅豆進行全基因體定序，共鑑定出約 100 萬個高品質單核苷酸多態性（SNP）。透過全基因體關聯分析（GWAS），我們辨識出兩個與開花時間有高度相關的候選基因：Vigan.04G378650.01（VaPHYA3）和Vigan.11G142800.01（VaGI2）。兩者皆為與豆科關鍵的開花基因存在同源關係，且都帶有非同義突變，其衍生型等位基因亦明顯集中在緯度比較高的品系，我們推測這些突變可能有助於降低光週期敏感性並促進紅豆在長日照條件下開花。此外，我們利用等位基因頻率變化軌跡進行建模，發現這些關鍵變異可能遠在一萬年前就出現了，並於約兩千年前迅速擴散，這個時間點剛好對應上日本的古墳時代。為進一步探討開花時間的演化過程，本研究首度將多基因風險分數應用至作物，重建族群層級的開花性狀演化動態。結果顯示，開花時間從數萬年前持續受到定向選汰的影響。綜合而言，本研究揭示了紅豆開花時間的遺傳結構與演化歷史，成果將有助於未來育種與作物適應性等相關研究上的應用。

Adzuki bean (Vigna angularis [Willd.] Ohwi and Ohashi, diploid, 2n = 22) is a traditional legume crop widely grown in East Asia and South Asia, celebrated for its nutrient-rich seeds, culinary versatility and appealing seed coat colouration. Today, its cultivation extends far beyond the natural distribution of its wild progenitor (V. angularis var. nipponensis), reaching higher latitude regions in China and Japan. As a short-day plant, adzuki bean is highly sensitive to photoperiod, typically flowers earlier under short-day conditions and delays flowering under long-day conditions. At higher latitudes, however, cultivated adzuki bean has to flower during long-day summers to complete the life cycle in time and avoid damages from freezing winters. While flowering time is a key trait for local adaptation and stable crop yield, its genetic architecture in aduki bean remains poorly understood. In this study, we conducted whole-genome sequencing on a geographically diverse panel of 454 cultivated and wild adzuki bean accessions across East Asia and northern South Asia, identifying about 1 million high-quality single nucleotide polymorphisms (SNPs). A genome-wide association study (GWAS) successfully revealed two novel candidate genes, Vigan.04G378650.01 (VaPHYA3) and Vigan.11G142800.01 (VaGI2), each harbouring nonsynonymous SNPs significantly associated with flowering time. Both genes are homologous to core flowering genes in legume. These nonsynonymous changes were enriched in accessions from higher latitude regions, likely contributing to their reduced photoperiod sensitivity and earlier flowering under long-day conditions. Allele trajectory modelling further suggests that the derived alleles may have been originated more than 10 thousand years ago (kya), with their frequencies increasing sharply in the past ~2 kya, during the Kofun period in Japan. Given that the complex genetic nature of flowering time and the challenges of tracing its history archaeologically, we further investigated the population-level evolution of flowering-time polygenic score, an unprecedented application in crops. This analysis captured long-term directional selection for earlier flowering over thousands of years. Altogether, these findings provide a new insight into the genetic basis and evolutionary history of flowering time in adzuki bean, offering potential resources for future breeding efforts and crop adaptation studies.