两个同源MYB转录因子在调控栽培草莓果实着色方面的功能差异

doi:10.1016/j.jia.2024.12.040

摘要/Abstract

摘要：

花青素是一种黄酮类色素，能够赋予水果和花朵鲜艳的颜色，在植物生理和人类健康中发挥着关键作用。MYB转录因子是花青素生物合成和积累的重要调控因子，但目前同源MYB转录因子在调控花青素含量上的功能差异尚不清晰。在草莓（Fragaria x ananassa）中，FaMYB44.1和FaMYB44.3是高度同源的MYB转录因子，定位于细胞核，被弱光条件明显诱导表达。然而，它们对果实花青素积累的影响不同。在‘BeniHoppe’和‘JianDe-Hong’两草莓品种中，FaMYB44.1通过转录抑制花青素积累所必需的FaF3H基因表达来抑制花青素合成。相比之下，FaMYB44.3不影响花青素含量变化。本研究全面解析了FaMYB44.1和FaMYB44.3在草莓果实花青素调控中的作用。通过阐明相关分子机制，本研究加深了我们对遗传和环境因素如何相互作用控制果实着色并提高其营养价值的理解。

Abstract:

Anthocyanins are the flavonoid pigments responsible for vibrant fruit and flower colors, and they also play key roles in both plant physiology and human health. MYB transcription factors are crucial regulators of anthocyanin biosynthesis and accumulation, but the functional differences of homologous MYB transcription factors in regulating anthocyanin content are still unclear. In strawberry (Fragaria×ananassa), FaMYB44.1 and FaMYB44.3 are highly homologous MYB transcription factors localized in the nucleus and can be significantly induced by weak light. However, they differ in their effects on anthocyanin accumulation in the fruits. FaMYB44.1 inhibits anthocyanin synthesis by transcriptionally suppressing FaF3H, which is essential for anthocyanin regulation, in the ‘BeniHoppe’ and ‘JianDe-Hong’ strawberry varieties. In contrast, FaMYB44.3 does not affect anthocyanin levels. This study provides a comprehensive overview of the roles of FaMYB44.1 and FaMYB44.3 in anthocyanin regulation in strawberry fruits. By elucidating the molecular mechanisms underlying their regulation, this study enhances our understanding of how the interactions between genetic and environmental factors control fruit pigmentation and enhance the nutritional value of the fruit.

Key words: strawberry , FaMYB44.1 , FaMYB44.3 , FaF3H , anthocyanin , transcriptional regulation

Lixia Sheng, Yuqi Zhang, Xiaoke Yang, Yujia Yin, Jianqiang Yu. 两个同源MYB转录因子在调控栽培草莓果实着色方面的功能差异[J]. Journal of Integrative Agriculture, 2025, 24(9): 3484-3493.

Lixia Sheng, Yuqi Zhang, Xiaoke Yang, Yujia Yin, Jianqiang Yu. Functional differences between two homologous MYB transcription factors in regulating fruit color in octoploid strawberry (Fragaria×ananassa)[J]. Journal of Integrative Agriculture, 2025, 24(9): 3484-3493.

参考文献

Aer ts R J, Barry T N, McNabb W C. 1999. Polyphenols and agriculture: Beneficial effects of proanthocyanidins in forages. Agriculture, Ecosystems & Environment, 75, 1–12.

Allan A C, Hellens R P, Laing W A. 2008. MYB transcription factors that colour our fruit. Trends in Plant Science, 13, 99–102.

Cai J, Mo X, Wen C, Gao Z, Chen X, Xue C. 2022. FvMYB79 positively regulates strawberry fruit softening via transcriptional activation of FvPME38. International Journal of Molecular Sciences, 23, 101.

Castillejo C, Waurich V, Wagner H, Ramos R, Oiza N, Muñoz P, Triviño J C, Caruana J, Liu Z, Cobo N, Hardigan M A, Knapp S, Vallarino J G, Osorio S, Martín-Pizarro C, Martín-Pizarro C, Pose D, Toivainen T, Hytonen T, Oh Y, Barbey C R, Whitaker V M, Lee S, Olbricht K, Sánchez-Sevilla J F, Amaya I. 2020. Allelic variation of MYB10 is the major force controlling natural variation in skin and flesh color in strawberry (Fragaria spp.) fruit. The Plant Cell, 32, 3723–3749.

Chen J, Wang Z B, Liu S D, Zhang S P, Ge C W, Shen Q, Ma H J, Zhang X M, Dong H L, Zhao X H, Liu R H, Pang C Y. 2021. Nitrogen stress inhibits root growth by regulating cell wall and hormone changes in cotton (Gossypium hirsutum L.). Journal of Agronomy and Crop Science, 207, 1006–1023.

Costa A G V, Garcia-Diaz D F, Jimenez P, Silva P I. 2013. Bioactive compounds and health benefits of exotic tropical red-black berries. Journal of Functional Foods, 5, 539–549.

Feng K, Xu Z S, Que F, Liu J X, Wang F, Xiong A S. 2018. An R2R3-MYB transcription factor, OjMYB1, functions in anthocyanin biosynthesis in Oenanthe javanica. Planta, 247, 301–315.

Hawkins C, Caruana J, Schiksnis E, Liu Z. 2016. Genome-scale DNA variant analysis and functional validation of a SNP underlying yellow fruit color in wild strawberry. Scientific Reports, 6, 29017.

Hichri I, Heppel S C, Pillet J, Léon C, Czemmel S, Delrot S, Lauvergeat V, Bogs J. 2010. The basic helix-loop-helix transcription factor MYC1 is involved in the regulation of the flavonoid biosynthesis pathway in grapevine. Molecular Plant, 3, 509–523.

Hiratsu K, Matsui K, Koyama T, Ohme-Takagi M. 2003. Dominant repression of target genes by chimeric repressors that include the EAR motif, a repression domain, in Arabidopsis. The Plant Journal, 34, 733–739.

Jaakola L. 2013. New insights into the regulation of anthocyanin biosynthesis in fruits. Trends in Plant Science, 18, 477–483.

Jia L, Clegg M T, Jiang T. 2003. Excess non-synonymous substitutions suggest that positive selection episodes occurred during the evolution of DNA-binding domains in the Arabidopsis R2R3-MYB gene family. Plant Molecular Biology, 52, 627–642.

Kagale S, Links M G, Rozwadowski K. 2010. Genome-wide analysis of ethylene-responsive element binding factor-associated amphiphilic repression motif-containing transcriptional regulators in Arabidopsis. Plant Physiology, 152, 1109–1134.

Kranz H D, Denekamp M, Greco R, Jin H, Leyva A, Meissner R C, Petroni K, Urzainqui A, Bevan M, Martin C, Smeekens S, Tonelli C, Paz-Ares J, Weisshaar B. 1998. Towards functional characterisation of the members of the R2R3-MYB gene family from Arabidopsis thaliana. The Plant Journal, 16, 263–276.

Kui L W, Bolitho K, Grafton K, Kortstee A, Karunairetnam S, McGhie T K, Espley R V, Hellens R P, Allan A C. 2010. An R2R3 MYB transcription factor associated with regulation of the anthocyanin biosynthetic pathway in Rosaceae. BMC Plant Biology, 10, 50.

Kui L W, McGhie T K, Wang M, Liu Y, Warren B, Storey R, Espley R V, Allan A C. 2014. Engineering the anthocyanin regulatory complex of strawberry (Fragaria vesca). Frontiers in Plant Science, 5, 651.

Mao W, Han Y, Chen Y, Sun M, Feng Q, Li L, Liu L, Zhang K, Wei L, Han Z, Li B. 2022. Low temperature inhibits anthocyanin accumulation in strawberry fruit by activating FvMAPK3-induced phosphorylation of FvMYB10 and degradation of Chalcone Synthase 1. The Plant Cell, 34, 1226–1249.

Medina-Puche L, Cumplido-Laso G, Amil-Ruiz F, Hoffmann T, Ring L, Rodríguez-Franco A, Caballero J L, Schwab W, Muñoz-Blanco J, Blanco-Portales R. 2014. MYB10 plays a major role in the regulation of flavonoid/phenylpropanoid metabolism during ripening of Fragaria×ananassa fruits. Journal of Experimental Botany, 65, 401–417.

Muhammad N, Luo Z, Zhao X, Yang M, Liu Z G, Liu M J. 2023. Transcriptome-wide expression analysis of MYB gene family leads to functional characterization of favonoid biosynthesis in fruit coloration of Ziziphus Mill. Frontiers in Plant Science, 14, 1171288.

Qiao Q, Edger P P, Xue L, Qiong L, Lu J, Zhang Y, Cao Q, Yocca A E, Platts A E, Knapp S J, Montagu M V, Peer Y V, Lei J, Zhang T. 2021. Evolutionary history and pan-genome dynamics of strawberry (Fragaria spp.). Proceedings of the National Academy of Sciences of the United States of America, 118, e2105431118.

Romero I, Fuertes A, Benito M J, Malpica J M, Leyva A, Paz-Ares J. 1998. More than 80R2R3-MYB regulatory genes in the genome of Arabidopsis thaliana. The Plant Journal, 14, 273–284.

Schaart J G, Dubos C, Romero De La Fuente I, Houwelingen A M M L, Vos R C H, Jonker H H, Xu W, Routaboul J, Lepiniec L, Bovy A G. 2013. Identification and characterization of MYB-bHLH-WD 40 regulatory complexes controlling proanthocyanidin biosynthesis in strawberry (Fragaria×ananassa) fruits. New Phytologist, 197, 454–467.

Shin R, Burch A Y, Huppert K A, Tiwari S B, Murphy A S, Guilfoyle T J, Schachtman D P. 2007. The Arabidopsis transcription factor MYB77 modulates auxin signal transduction. The Plant Cell, 19, 2440–2453.

Stracke R, Werber M, Weisshaar B. 2001. The R2R3-MYB gene family in Arabidopsis thaliana. Current Opinion in Plant Biology, 4, 447–456.

Wang F, Yang F, Zhu D, Saniboere B, Zhou B, Peng D. 2024. MYB44 plays key roles in regulating plant responses to abiotic and biotic stress, metabolism, and development. Journal of Plant Biochemistry and Biotechnology, 33, 462–473.

Wang H, Zhang H, Yang Y, Li M, Zhang Y, Liu J, Dong J, Li J, Butelli E, Xue Z, Wang A, Wang G, Martin C, Jin W. 2020. The control of red colour by a family of MYB transcription factors in octoploid strawberry (Fragaria×ananassa) fruits. Plant Biotechnology Journal, 18, 1169–1184.

Wang L S, Stoner G D. 2008. Anthocyanins and their role in cancer prevention. Cancer Letters, 269, 281–290.

Wang S, Shi M, Zhang Y, Pan Z, Xie X, Zhang L, Sun P, Feng H, Xue H, Fang C, Zhao J. 2022. The R2R3-MYB transcription factor FaMYB63 participates in regulation of eugenol production in strawberry. Plant Physiology, 188, 2146–2165.

Wang Z D, Li X X, Yao X H, Ma J B, Lu K, An Y Y, Sun Z M, Wang Q, Zhou M, Qin L N, Zhang L Y, Zou S S, Chen L, Song C F, Dong H S, Zhang M X, Chen X C. 2023. MYB44 regulates PTI by promoting the expression of EIN2 and MPK3/6 in Arabidopsis. Plant Communications, 4, 2590–3462.

Wei L Z, Mao W W, Jia M R, Xing S N, Ali U, Zhao Y Y, Chen Y T, Cao M L, Dai Z R, Zhang K. 2018. FaMYB44.2, a transcriptional repressor, negatively regulates sucrose accumulation in strawberry receptacles through interplay with FaMYB10. Journal of Experimental Botany, 69, 4805–4820.

Wu R, Wang Y, Wu T, Xu X, Han Z. 2018. Functional characterisation of MdMYB44 as a negative regulator in the response to cold and salt stress in apple calli. The Journal of Horticultural Science and Biotechnology, 93, 347–355.

Xu P, Li X, Fan J, Tian S, Cao M, Lin A, Gao Q, Xiao K, Wang C, Kuang H, Lian H. 2023. An arginine-to-histidine mutation in flavanone-3-hydroxylase results in pink strawberry fruits. Plant Physiology, 193, 1849–1865.

Xu P, Wu L, Cao M, Ma C, Xiao K, Li Y, Lian H. 2021. Identification of MBW complex components implicated in the biosynthesis of flavonoids in woodland strawberry. Frontiers in Plant Science, 12, 774943.

Xu P Y, Xu L, Xu H F, He X W, He P, Chang Y S, Wang S, Zheng W Y, Wang C Z, Chen X, Li L G, Wang H B. 2023. MdWRKY40is directly promotes anthocyanin accumulation and blocks MdMYB15L, the repressor of MdCBF2, which improves cold tolerance in apple. Journal of Integrative Agriculture, 22, 1704–1719.

Yuan J C, Liu X X, Zhao H, Wang Y, Wei X, Wang P, Zhan J J, Liu L S, Li F G, Ge X Y. 2023. GhRCD1 regulates cotton somatic embryogenesis by modulating the GhMYC3–GhMYB44–GhLBD18 transcriptional cascade. New Phytologist, 240, 207–223.

Yu J Q, Gu K D, Zhang L L, Sun C H, Zhang Q Y, Wang J H, Wang C K, Wang W Y, Du M C, Hu D G. 2022. MdbHLH3 modulates apple soluble sugar content by activating phosphofructokinase gene expression. Journal of Integrative Plant Biology, 64, 884–900.

Zhou X J, Zha M R, Huang J, Li L, Imran M, Zhang C K. 2017. StMYB44 negatively regulates phosphate transport by suppressing expression of PHOSPHATE1 in potato. Journal of Experimental Botany, 68, 1265–1281.