An investigation of DNA methylation, chromatin accessibility and histone modification changes during fleshy fruit ripening

Ph.D.Fleshy fruits are classically categorized into two groups: climacteric fruits, which present increased rate of respiration and induce enhanced and autocatalytic ethylene production during ripening; and non-climacteric fruits, which don’t undergo these transitions throughout their development. Although ethylene was known to be essential for the ripening of climacteric fruits, the mechanisms of autocatalytic ethylene production and activation of downstream ripening genes are largely unknown. In tomato, a representative of climacteric fruits, DNA methylation serves as a checkpoint to prevent ripening before seed maturation. It is unclear whether any other silencing epigenetic mark such as H3K27me3 is implicated in fruit ripening. In the history of angiosperms, climacteric fruits have arisen multiple times. To what extent the ethylenebased ripening regulatory circuits and the associated epigenetic regulation are conserved among angiosperms remains to be elucidated.In this study, more than 130 transcriptome, 39 accessible chromatin, 48 H3K27me3 modification and 36 DNA methylation profiles of leaf and fruit or fruit resembling tissues of eleven fleshy fruit species and two dry fruit species were analyzed. Three types of transcriptional positive feedback circuits responsible for autocatalytic ethylene production and activation of many downstream ripening processes were revealed. MADS transcription factors originally dictating floral organ identity or a NAC transcription factor originally related to senescence servers as the key components of these circuits. Epigenome changes during fruit development and ripening indicate that H3K27me3 might play a conserved role in restricting key circuit genes and their close homologs in non-climacteric and dry fruits, while the role of DNA methylation in controlling these ripening circuits seems not conserved. The lack of a mechanism able to activate ACS genes that are epigenetically repressed, by H3K27me3 in particular, precludes non-climacteric fruits from forming similar positive feedback circuits. These findings offer new insights into the mechanisms of climacteric fruit ripening.肉質果實傳統上被分為呼吸躍變型和非呼吸躍變型。前者在成熟過程中呈現出更快的呼吸速率，以及增強的、自我催化式的乙烯合成；而後者在整個發育過程中不呈現類似的轉變。儘管乙烯早已被證明在呼吸躍變型果實的成熟過程中不可或缺，該過程中實現自我催化式的乙烯合成以及啟動果實成熟下游基因的分子機理尚不清楚。在呼吸躍變型果實的代表-番茄中，DNA甲基化阻止成熟過程在種子成熟之前被啟動。目前仍然不清楚其他具有轉錄抑制效應的表觀遺傳修飾，例如H3K27me3，是否也參與調控果實的成熟。被子植物的進化過程曾多次地、獨立地形成呼吸躍變型果實。其進化出來的依賴于乙烯的果實成熟調控通路以及相關的表觀遺傳調控在眾多物種之間的保守性仍有待研究。本研究分析了超過130 個轉錄組，39 個開放性染色質組，48 個H3K27me3 組蛋白修飾組和36 個DNA 甲基化組。這些數據來自于11 個肉質果實物種和2 個乾果物種的葉片、果實或者類似于果實的組織。我們揭示了3 種負責乙烯自我催化合成和激活果實成熟下游通路的正反饋轉錄調控通路。原先控制花器官發育的數個MADS 轉錄因子或者一個于衰老相關的NAC 轉錄因子是這些通路的核型成員之一。果實發育和成熟過程中表觀基因組的動態變化表明，H3K27me3在抑制這些通路中的核心成員以及它們在非躍變型果實和乾果中的近緣同源基因方面發揮著保守性作用，而DNA 甲基化在調控這些通路方面的作用趨於分化。非躍變型果實都缺乏一個有效機制來激活被表觀遺傳因素尤其是H3K27me3 抑制的ACS 基因，導致它們無法形成類似的正反饋調控通路。這些發現提供了對躍變型果實成熟機制的新認識。Yu, Sheng.Thesis Ph.D. Chinese University of Hong Kong 2019.Includes bibliographical references (leaves 99-112).Abstracts also in Chinese.Title from PDF title page (viewed on 12, January, 2021)