亞洲秋海棠氣孔簇和下皮層的適應演化

Abstract

由二或多個氣孔聚集成簇的非接觸型氣孔簇 (non-contiguous stomatal cluster) 是非常特殊的氣孔排列形式，主要出現在菊類及薔薇類中，例如秋海棠屬中的某些類群。野外觀察、解剖學和生理生態研究顯示氣孔簇相較於單生氣孔能使秋海棠有較高的水分使用效率和更大的共用氣室，可能與適應乾旱環境有關。值得一提的是在秋海棠屬中，許多具有氣孔簇的類群也有葉片下皮層 (hypodermis)，而葉片下皮層也被認為是植物適應乾旱的特徵之一。然而，不管是氣孔簇或葉片下皮層對於秋海棠的適應意義，皆只由研究極為少數的種類進而提出假說，是否具有普遍性，需要大尺度的取樣來支持。本研究使用標靶捕獲的次世代定序策略，重建高解析度的亞洲秋海棠親緣關係樹，並收集特徵資料，進行親緣比較分析，以檢驗氣孔簇和葉片下皮層幫助秋海棠適應乾旱環境的假說。結果顯示獨立的支序重複地轉為氣孔簇和獲得葉片下皮層，且氣孔簇和葉片下皮層之間具有顯著的親緣相關性，顯示此二特徵極可能具適應性，且為適應相似的特定環境。兩者皆具極顯著的親緣訊號，暗示秋海棠明顯的親緣棲位保守性。亞洲秋海棠主要獲得氣孔簇的事件發生在岩生的 Sect. Baryandra 和 Sect. Jackia，而岩生植物時常面臨乾旱逆境，支持前人之氣孔簇乾旱適應假說。藉由整合親緣基因體學和植物解剖學，本研究結果對於多樣性極高的秋海棠屬，提供了生態、演化和種化的新觀點。

The non-contiguous stomatal cluster, a unique arrangement of anatomic pattern formed by the grouping of two or more stomata, is only observed in some clades of Asterids and Rosids such as Begonia. Based on field observations, anatomical studies, and ecophysiological data, it is known that the stomatal cluster in Begonia provides higher water usage efficiency and larger substomatal cavity than singular stomata. Consequently, this unique arrangement has been hypothesized as an adaptation for growing in arid environments. In Begonia, many taxa with stomatal cluster also possess the hypodermis, which has been recognized as an adaptation for drought resistance. However, since the adaptive significance of the stomatal cluster and/or hypodermis in Begonia was hitherto observed only on a few species, studies with a larger sampling scale are necessary to confirm the general applicability of this hypothesis. In this study, we reconstruct a highly resolved phylogenomic tree of Asian Begonia using Hyb-Seq data, and collect character data for phylogenetic comparative analyses to test the hypothesis. We found a significant phylogenetic correlation between the stomatal cluster and hypodermis in Begonia and the gain of these two characters occurred repeatedly across the phylogeny. These findings suggest that the two characters might be adaptive and specialized for similar specific environments. Additionally, the strong and significant phylogenetic signals detected in both the leaf anatomical traits and habitat types imply the high degree of phylogenetic niche conservatism in Begonia. The transition of singular stomata into stomatal clusters of Asian Begonia occurred mainly in Sect. Baryandra and Sect. Jackia whose species are predominantly lithophytic and often face drought stress, thus supporting the previous drought adaptation hypothesis regarding the adaptive significance of stomatal cluster. By integrating phylogenomics and plant anatomy, our results provide new insights into the ecology, evolution and speciation of the mega-diverse Begonia.