The chromosome-level holly (Ilex latifolia) genome reveals key enzymes in triterpenoid saponin biosynthesis and fruit color change

The Ilex L. (hollies) genus of Aquifoliaceae shows high species diversity in tropical and subtropical regions of Asia and South America. Throughout the range of the genus, Ilex species have been widely used in beverage and medicine production and as ornamentals. Here, we assembled a high-quality, ch...

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Main Authors: Ke-Wang Xu, Xue-Fen Wei, Chen-Xue Lin, Min Zhang, Qiang Zhang, Peng Zhou, Yan-Ming Fang, Jia-Yu Xue, Yi-Fan Duan
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-08-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2022.982323/full
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author Ke-Wang Xu
Xue-Fen Wei
Chen-Xue Lin
Min Zhang
Min Zhang
Qiang Zhang
Peng Zhou
Yan-Ming Fang
Jia-Yu Xue
Yi-Fan Duan
author_facet Ke-Wang Xu
Xue-Fen Wei
Chen-Xue Lin
Min Zhang
Min Zhang
Qiang Zhang
Peng Zhou
Yan-Ming Fang
Jia-Yu Xue
Yi-Fan Duan
author_sort Ke-Wang Xu
collection DOAJ
description The Ilex L. (hollies) genus of Aquifoliaceae shows high species diversity in tropical and subtropical regions of Asia and South America. Throughout the range of the genus, Ilex species have been widely used in beverage and medicine production and as ornamentals. Here, we assembled a high-quality, chromosome-level genome of Ilex latifolia, which has extremely high economic value because of its useful secondary metabolite production and the high ornamental value of its decorative red berries. The 99.8% genome sequence was anchored to 20 pseudochromosomes, with a total length of 766.02 Mb and a scaffold N50 of 33.45 Mb. Based on the comparative genomic analysis of 14 angiosperm species, we recovered I. latifolia as the sister group to all other campanulids. Two whole-genome duplication (WGD) events were identified in hollies: one shared ancient WGD in the ancestor of all eudicots and a recent and independent WGD in hollies. We performed a genome-wide search to screen candidate genes involved in the biosynthesis of pentacyclic triterpenoid saponins in I. latifolia. Three subfamilies of CYP450 (CYP71A, CYP72A, and CYP716A) appear to have expanded. The transcriptomic analysis of I. latifolia leaves at five developmental stages revealed that two CYP716A genes and one CYP72A gene probably play important roles in this biosynthetic pathway. In addition, we totally identified 12 genes in the biosynthesis pathways of pelargonidin and cyanidin and observed their differential expression in green and red fruit pericarps, suggesting an association between pelargonidin and cyanidin biosynthesis and fruit pericarp color change. The accumulation of pelargonidin and cyanidin is expected to play an important role in the ornamental value of I. latifolia. Altogether, this study elucidated the molecular basis of the medicinal and ornamental value of I. latifolia, providing a data basis and promising clues for further applications.
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spelling doaj.art-6bb612cd954b4508a35c51c5f7d434822022-12-22T02:15:23ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2022-08-011310.3389/fpls.2022.982323982323The chromosome-level holly (Ilex latifolia) genome reveals key enzymes in triterpenoid saponin biosynthesis and fruit color changeKe-Wang Xu0Xue-Fen Wei1Chen-Xue Lin2Min Zhang3Min Zhang4Qiang Zhang5Peng Zhou6Yan-Ming Fang7Jia-Yu Xue8Yi-Fan Duan9Key Laboratory of National Forestry and Grassland Administration on Subtropical Forest Biodiversity Conservation, Co-innovation Center for Sustainable Forestry in Southern China, College of Biology and the Environment, Nanjing Forestry University, Nanjing, ChinaCollege of Horticulture, Academy for Advanced Interdisciplinary Studies, Nanjing Agricultural University, Nanjing, ChinaKey Laboratory of National Forestry and Grassland Administration on Subtropical Forest Biodiversity Conservation, Co-innovation Center for Sustainable Forestry in Southern China, College of Biology and the Environment, Nanjing Forestry University, Nanjing, ChinaKey Laboratory of National Forestry and Grassland Administration on Subtropical Forest Biodiversity Conservation, Co-innovation Center for Sustainable Forestry in Southern China, College of Biology and the Environment, Nanjing Forestry University, Nanjing, ChinaJiangsu Academy of Forestry, Nanjing, ChinaKey Laboratory of National Forestry and Grassland Administration on Subtropical Forest Biodiversity Conservation, Co-innovation Center for Sustainable Forestry in Southern China, College of Biology and the Environment, Nanjing Forestry University, Nanjing, ChinaJiangsu Academy of Forestry, Nanjing, ChinaKey Laboratory of National Forestry and Grassland Administration on Subtropical Forest Biodiversity Conservation, Co-innovation Center for Sustainable Forestry in Southern China, College of Biology and the Environment, Nanjing Forestry University, Nanjing, ChinaCollege of Horticulture, Academy for Advanced Interdisciplinary Studies, Nanjing Agricultural University, Nanjing, ChinaKey Laboratory of National Forestry and Grassland Administration on Subtropical Forest Biodiversity Conservation, Co-innovation Center for Sustainable Forestry in Southern China, College of Biology and the Environment, Nanjing Forestry University, Nanjing, ChinaThe Ilex L. (hollies) genus of Aquifoliaceae shows high species diversity in tropical and subtropical regions of Asia and South America. Throughout the range of the genus, Ilex species have been widely used in beverage and medicine production and as ornamentals. Here, we assembled a high-quality, chromosome-level genome of Ilex latifolia, which has extremely high economic value because of its useful secondary metabolite production and the high ornamental value of its decorative red berries. The 99.8% genome sequence was anchored to 20 pseudochromosomes, with a total length of 766.02 Mb and a scaffold N50 of 33.45 Mb. Based on the comparative genomic analysis of 14 angiosperm species, we recovered I. latifolia as the sister group to all other campanulids. Two whole-genome duplication (WGD) events were identified in hollies: one shared ancient WGD in the ancestor of all eudicots and a recent and independent WGD in hollies. We performed a genome-wide search to screen candidate genes involved in the biosynthesis of pentacyclic triterpenoid saponins in I. latifolia. Three subfamilies of CYP450 (CYP71A, CYP72A, and CYP716A) appear to have expanded. The transcriptomic analysis of I. latifolia leaves at five developmental stages revealed that two CYP716A genes and one CYP72A gene probably play important roles in this biosynthetic pathway. In addition, we totally identified 12 genes in the biosynthesis pathways of pelargonidin and cyanidin and observed their differential expression in green and red fruit pericarps, suggesting an association between pelargonidin and cyanidin biosynthesis and fruit pericarp color change. The accumulation of pelargonidin and cyanidin is expected to play an important role in the ornamental value of I. latifolia. Altogether, this study elucidated the molecular basis of the medicinal and ornamental value of I. latifolia, providing a data basis and promising clues for further applications.https://www.frontiersin.org/articles/10.3389/fpls.2022.982323/fullAquifolialeswhole-genome sequencinggenome evolutionpentacyclic triterpenoid saponinsanthocyanidins biosynthesis genesholly
spellingShingle Ke-Wang Xu
Xue-Fen Wei
Chen-Xue Lin
Min Zhang
Min Zhang
Qiang Zhang
Peng Zhou
Yan-Ming Fang
Jia-Yu Xue
Yi-Fan Duan
The chromosome-level holly (Ilex latifolia) genome reveals key enzymes in triterpenoid saponin biosynthesis and fruit color change
Frontiers in Plant Science
Aquifoliales
whole-genome sequencing
genome evolution
pentacyclic triterpenoid saponins
anthocyanidins biosynthesis genes
holly
title The chromosome-level holly (Ilex latifolia) genome reveals key enzymes in triterpenoid saponin biosynthesis and fruit color change
title_full The chromosome-level holly (Ilex latifolia) genome reveals key enzymes in triterpenoid saponin biosynthesis and fruit color change
title_fullStr The chromosome-level holly (Ilex latifolia) genome reveals key enzymes in triterpenoid saponin biosynthesis and fruit color change
title_full_unstemmed The chromosome-level holly (Ilex latifolia) genome reveals key enzymes in triterpenoid saponin biosynthesis and fruit color change
title_short The chromosome-level holly (Ilex latifolia) genome reveals key enzymes in triterpenoid saponin biosynthesis and fruit color change
title_sort chromosome level holly ilex latifolia genome reveals key enzymes in triterpenoid saponin biosynthesis and fruit color change
topic Aquifoliales
whole-genome sequencing
genome evolution
pentacyclic triterpenoid saponins
anthocyanidins biosynthesis genes
holly
url https://www.frontiersin.org/articles/10.3389/fpls.2022.982323/full
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