LbNR-Derived Nitric Oxide Delays Lycium Fruit Coloration by Transcriptionally Modifying Flavonoid Biosynthetic Pathway

Anthocyanin-derived fleshy fruit pigmentation has become an excellent system for studying the regulatory network underlying fruit ripening and quality. The transcriptional control of anthocyanin biosynthesis by MYB–bHLH–WDR complexes has been well established, but the intermediate signals through wh...

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Main Authors: Gen Li, Beibei Qin, Shuodan Li, Yue Yin, Jianhua Zhao, Wei An, Youlong Cao, Zixin Mu
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-08-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fpls.2020.01215/full
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spelling doaj-3e309abbdf654fdd998f53ddbbd6be4a2020-11-25T04:01:30ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2020-08-011110.3389/fpls.2020.01215538076LbNR-Derived Nitric Oxide Delays Lycium Fruit Coloration by Transcriptionally Modifying Flavonoid Biosynthetic PathwayGen Li0Beibei Qin1Shuodan Li2Yue Yin3Jianhua Zhao4Wei An5Youlong Cao6Zixin Mu7College of Life Sciences, Northwest A&F University, Yangling, ChinaCollege of Life Sciences, Northwest A&F University, Yangling, ChinaCollege of Grassland Agriculture, Northwest A&F University, Yangling, ChinaNational Wolfberry Engineering Research Center, Ningxia Academy of Agriculture and Forestry Sciences, Yinchuan, ChinaNational Wolfberry Engineering Research Center, Ningxia Academy of Agriculture and Forestry Sciences, Yinchuan, ChinaNational Wolfberry Engineering Research Center, Ningxia Academy of Agriculture and Forestry Sciences, Yinchuan, ChinaNational Wolfberry Engineering Research Center, Ningxia Academy of Agriculture and Forestry Sciences, Yinchuan, ChinaCollege of Life Sciences, Northwest A&F University, Yangling, ChinaAnthocyanin-derived fleshy fruit pigmentation has become an excellent system for studying the regulatory network underlying fruit ripening and quality. The transcriptional control of anthocyanin biosynthesis by MYB–bHLH–WDR complexes has been well established, but the intermediate signals through which the environmental or developmental cues regulate these transcription factors remain poorly understood. Here we found that nitric oxide (NO) production during Lycium fruit ripening decreased progressively presenting a negative relationship with anthocyanins. After cloning of the nitric reductase (NR) gene from Lyciumbarbarum (LbNR) plants, we demonstrated that LbNR-derived NO partially inhibited anthocyanin biosynthesis but enhanced proanthocyanidin (PA) accumulation, and delayed fruit coloration. Application of the NO donor, sodium nitroprusside (SNP), produced a similar effect. The endogenous or exogenous NO downregulated the transcripts both of the regulatory genes and the structural genes that related to anthocyanin biosynthesis, while upregulated both of those genes that related to PA biosynthesis. Given there is a significant negative relationship between the levels of anthocyanins and PAs during Lycium fruit ripening, NO not only inhibited anthocyanin de novo biosynthesis but redirected the flavonoid biosynthetic pathway from anthocyanins to PA production. Two types of LrMYB transcription factors of opposite nature, namely anthocyanin-specific and PA-specific, which belong to the R2R3-MYB subfamily and 1R-MYB subfamily, respectively, were identified from L. ruthenicum fruits. It was further found that NO acts by antagonizing the ABA signaling, a phytohormone we have previously shown playing a positive role in Lycium fruit coloration. Our results provided particularly novel information about NO–ABA–anthocyanin interplay during Lycium fruit development and ripening, which may fill a gap between the developmental cues and the transcriptional regulation of anthocyanin biosynthesis.https://www.frontiersin.org/article/10.3389/fpls.2020.01215/fullLyciumfruit ripeningnitric oxide (NO)nitric reductase (NR)anthocyaninsproanthocyanidins
collection DOAJ
language English
format Article
sources DOAJ
author Gen Li
Beibei Qin
Shuodan Li
Yue Yin
Jianhua Zhao
Wei An
Youlong Cao
Zixin Mu
spellingShingle Gen Li
Beibei Qin
Shuodan Li
Yue Yin
Jianhua Zhao
Wei An
Youlong Cao
Zixin Mu
LbNR-Derived Nitric Oxide Delays Lycium Fruit Coloration by Transcriptionally Modifying Flavonoid Biosynthetic Pathway
Frontiers in Plant Science
Lycium
fruit ripening
nitric oxide (NO)
nitric reductase (NR)
anthocyanins
proanthocyanidins
author_facet Gen Li
Beibei Qin
Shuodan Li
Yue Yin
Jianhua Zhao
Wei An
Youlong Cao
Zixin Mu
author_sort Gen Li
title LbNR-Derived Nitric Oxide Delays Lycium Fruit Coloration by Transcriptionally Modifying Flavonoid Biosynthetic Pathway
title_short LbNR-Derived Nitric Oxide Delays Lycium Fruit Coloration by Transcriptionally Modifying Flavonoid Biosynthetic Pathway
title_full LbNR-Derived Nitric Oxide Delays Lycium Fruit Coloration by Transcriptionally Modifying Flavonoid Biosynthetic Pathway
title_fullStr LbNR-Derived Nitric Oxide Delays Lycium Fruit Coloration by Transcriptionally Modifying Flavonoid Biosynthetic Pathway
title_full_unstemmed LbNR-Derived Nitric Oxide Delays Lycium Fruit Coloration by Transcriptionally Modifying Flavonoid Biosynthetic Pathway
title_sort lbnr-derived nitric oxide delays lycium fruit coloration by transcriptionally modifying flavonoid biosynthetic pathway
publisher Frontiers Media S.A.
series Frontiers in Plant Science
issn 1664-462X
publishDate 2020-08-01
description Anthocyanin-derived fleshy fruit pigmentation has become an excellent system for studying the regulatory network underlying fruit ripening and quality. The transcriptional control of anthocyanin biosynthesis by MYB–bHLH–WDR complexes has been well established, but the intermediate signals through which the environmental or developmental cues regulate these transcription factors remain poorly understood. Here we found that nitric oxide (NO) production during Lycium fruit ripening decreased progressively presenting a negative relationship with anthocyanins. After cloning of the nitric reductase (NR) gene from Lyciumbarbarum (LbNR) plants, we demonstrated that LbNR-derived NO partially inhibited anthocyanin biosynthesis but enhanced proanthocyanidin (PA) accumulation, and delayed fruit coloration. Application of the NO donor, sodium nitroprusside (SNP), produced a similar effect. The endogenous or exogenous NO downregulated the transcripts both of the regulatory genes and the structural genes that related to anthocyanin biosynthesis, while upregulated both of those genes that related to PA biosynthesis. Given there is a significant negative relationship between the levels of anthocyanins and PAs during Lycium fruit ripening, NO not only inhibited anthocyanin de novo biosynthesis but redirected the flavonoid biosynthetic pathway from anthocyanins to PA production. Two types of LrMYB transcription factors of opposite nature, namely anthocyanin-specific and PA-specific, which belong to the R2R3-MYB subfamily and 1R-MYB subfamily, respectively, were identified from L. ruthenicum fruits. It was further found that NO acts by antagonizing the ABA signaling, a phytohormone we have previously shown playing a positive role in Lycium fruit coloration. Our results provided particularly novel information about NO–ABA–anthocyanin interplay during Lycium fruit development and ripening, which may fill a gap between the developmental cues and the transcriptional regulation of anthocyanin biosynthesis.
topic Lycium
fruit ripening
nitric oxide (NO)
nitric reductase (NR)
anthocyanins
proanthocyanidins
url https://www.frontiersin.org/article/10.3389/fpls.2020.01215/full
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