The Transcription Factor CitZAT5 Modifies Sugar Accumulation and Hexose Proportion in Citrus Fruit

Overview

Journal Plant Physiol

Specialty Physiology

Date 2023 Mar 13

PMID 36911987

Authors

Heting Fang

Yanna Shi

Shengchao Liu

Rong Jin

Jun Sun

Donald Grierson

Shaojia Li

Kunsong Chen

Affiliations

Soon will be listed here.

Abstract

Sugars are fundamental to plant developmental processes. For fruits, the accumulation and proportion of sugars play crucial roles in the development of quality and attractiveness. In citrus (Citrus reticulata Blanco.), we found that the difference in sweetness between mature fruits of "Gongchuan" and its bud sport "Youliang" is related to hexose contents. Expression of a SuS (sucrose synthase) gene CitSUS5 and a SWEET (sugars will eventually be exported transporter) gene CitSWEET6, characterized by transcriptome analysis at different developmental stages of these 2 varieties, revealed higher expression levels in "Youliang" fruit. The roles of CitSUS5 and CitSWEET6 were investigated by enzyme activity and transient assays. CitSUS5 promoted the cleavage of sucrose to hexoses, and CitSWEET6 was identified as a fructose transporter. Further investigation identified the transcription factor CitZAT5 (ZINC FINGER OF ARABIDOPSIS THALIANA) that contributes to sucrose metabolism and fructose transportation by positively regulating CitSUS5 and CitSWEET6. The role of CitZAT5 in fruit sugar accumulation and hexose proportion was investigated by homologous transient CitZAT5 overexpression, -VIGS, and -RNAi. CitZAT5 modulates the hexose proportion in citrus by mediating CitSUS5 and CitSWEET6 expression, and the molecular mechanism explained the differences in sugar composition of "Youliang" and "Gongchuan" fruit.

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References

Li X, Guo W, Li J, Yue P, Bu H, Jiang J . Histone Acetylation at the Promoter for the Transcription Factor PuWRKY31 Affects Sucrose Accumulation in Pear Fruit. Plant Physiol. 2020; 182(4):2035-2046. PMC: 7140945. DOI: 10.1104/pp.20.00002. View

Griffing L . FRET analysis of transmembrane flipping of FM4-64 in plant cells: is FM4-64 a robust marker for endocytosis?. J Microsc. 2008; 231(2):291-8. DOI: 10.1111/j.1365-2818.2008.02042.x. View

Kelebek H, Selli S . Determination of volatile, phenolic, organic acid and sugar components in a Turkish cv. Dortyol (Citrus sinensis L. Osbeck) orange juice. J Sci Food Agric. 2011; 91(10):1855-62. DOI: 10.1002/jsfa.4396. View

Coleman H, Yan J, Mansfield S . Sucrose synthase affects carbon partitioning to increase cellulose production and altered cell wall ultrastructure. Proc Natl Acad Sci U S A. 2009; 106(31):13118-23. PMC: 2722352. DOI: 10.1073/pnas.0900188106. View

Deng Y, Wang J, Zhang Z, Wu Y . Transactivation of Sus1 and Sus2 by Opaque2 is an essential supplement to sucrose synthase-mediated endosperm filling in maize. Plant Biotechnol J. 2020; 18(9):1897-1907. PMC: 7415785. DOI: 10.1111/pbi.13349. View

Li Y, Liu H, Yao X, Wang J, Feng S, Sun L . Hexose transporter CsSWEET7a in cucumber mediates phloem unloading in companion cells for fruit development. Plant Physiol. 2021; 186(1):640-654. PMC: 8154047. DOI: 10.1093/plphys/kiab046. View

Hu L, Zhang F, Song S, Yu X, Ren Y, Zhao X . , a Hexose Transporter from Cucumber ( L.), Affects Sugar Metabolism and Improves Cold Tolerance in Arabidopsis. Int J Mol Sci. 2022; 23(7). PMC: 8999130. DOI: 10.3390/ijms23073886. View

Rehman A, Wang N, Peng Z, He S, Zhao Z, Gao Q . Identification of CH subfamily ZAT genes in Gossypium species reveals GhZAT34 and GhZAT79 enhanced salt tolerance in Arabidopsis and cotton. Int J Biol Macromol. 2021; 184:967-980. DOI: 10.1016/j.ijbiomac.2021.06.166. View

Chen J, Liu Y, Ni J, Wang Y, Bai Y, Shi J . OsPHF1 regulates the plasma membrane localization of low- and high-affinity inorganic phosphate transporters and determines inorganic phosphate uptake and translocation in rice. Plant Physiol. 2011; 157(1):269-78. PMC: 3165875. DOI: 10.1104/pp.111.181669. View

10.

Zhang X, Wang W, Du L, Xie J, Yao Y, Sun G . Expression patterns, activities and carbohydrate-metabolizing regulation of sucrose phosphate synthase, sucrose synthase and neutral invertase in pineapple fruit during development and ripening. Int J Mol Sci. 2012; 13(8):9460-9477. PMC: 3431806. DOI: 10.3390/ijms13089460. View

11.

Peng X, Wang Q, Wang Y, Cheng B, Zhao Y, Zhu S . A maize NAC transcription factor, ZmNAC34, negatively regulates starch synthesis in rice. Plant Cell Rep. 2019; 38(12):1473-1484. DOI: 10.1007/s00299-019-02458-2. View

12.

Vogel J, Zarka D, Van Buskirk H, Fowler S, Thomashow M . Roles of the CBF2 and ZAT12 transcription factors in configuring the low temperature transcriptome of Arabidopsis. Plant J. 2005; 41(2):195-211. DOI: 10.1111/j.1365-313X.2004.02288.x. View

13.

Bush D . Identifying the pathways that control resource allocation in higher plants. Proc Natl Acad Sci U S A. 2020; 117(16):8669-8671. PMC: 7183192. DOI: 10.1073/pnas.2002581117. View

14.

Chen L, Hou B, Lalonde S, Takanaga H, Hartung M, Qu X . Sugar transporters for intercellular exchange and nutrition of pathogens. Nature. 2010; 468(7323):527-32. PMC: 3000469. DOI: 10.1038/nature09606. View

15.

Tang H, Bi H, Liu B, Lou S, Song Y, Tong S . WRKY33 interacts with WRKY12 protein to up-regulate RAP2.2 during submergence induced hypoxia response in Arabidopsis thaliana. New Phytol. 2020; 229(1):106-125. DOI: 10.1111/nph.17020. View

16.

Wei W, Cheng M, Ba L, Zeng R, Luo D, Qin Y . Pitaya HpWRKY3 Is Associated with Fruit Sugar Accumulation by Transcriptionally Modulating Sucrose Metabolic Genes and . Int J Mol Sci. 2019; 20(8). PMC: 6514986. DOI: 10.3390/ijms20081890. View

17.

Wang K, Ding Y, Cai C, Chen Z, Zhu C . The role of C2H2 zinc finger proteins in plant responses to abiotic stresses. Physiol Plant. 2018; 165(4):690-700. DOI: 10.1111/ppl.12728. View

18.

Mathan J, Singh A, Ranjan A . Sucrose transport in response to drought and salt stress involves ABA-mediated induction of OsSWEET13 and OsSWEET15 in rice. Physiol Plant. 2020; 171(4):620-637. DOI: 10.1111/ppl.13210. View

19.

Riesmeier J, Willmitzer L, Frommer W . Isolation and characterization of a sucrose carrier cDNA from spinach by functional expression in yeast. EMBO J. 1992; 11(13):4705-13. PMC: 556945. DOI: 10.1002/j.1460-2075.1992.tb05575.x. View

20.

Wang Z, Wei X, Yang J, Li H, Ma B, Zhang K . Heterologous expression of the apple hexose transporter MdHT2.2 altered sugar concentration with increasing cell wall invertase activity in tomato fruit. Plant Biotechnol J. 2019; 18(2):540-552. PMC: 6953210. DOI: 10.1111/pbi.13222. View