MdHIR Proteins Repress Anthocyanin Accumulation by Interacting with the MdJAZ2 Protein to Inhibit Its Degradation in Apples

Overview

Journal Sci Rep

Specialty Science

Date 2017 Mar 21

PMID 28317851

Citations 5

Authors

Ke-Qin Chen

Xian-Yan Zhao

Xiu-Hong An

Yi Tian

Dan-Dan Liu

Chun-Xiang You

Yu-Jin Hao

Affiliations

Soon will be listed here.

Abstract

In higher plants, jasmonate ZIM-domain (JAZ) proteins negatively regulate the biosynthesis of anthocyanins by interacting with bHLH transcription factors. However, it is largely unknown if and how other regulators are involved in this process. In this study, the apple MdJAZ2 protein was characterized in regards to its function in the negative regulation of anthocyanin accumulation and peel coloration. MdJAZ2 was used as a bait to screen a cDNA library using the yeast two-hybrid method. The hypersensitive induced reaction (HIR) proteins, MdHIR2 and MdHIR4, were obtained from this yeast two-hybrid. The ZIM domain of MdJAZ2 and the PHB domain of the MdHIR proteins are necessary for their interactions. The interactions were further verified using an in vitro pull-down assay. Subsequently, immunoblotting assays demonstrated that MdHIR4 enhanced the stability of the MdJAZ2-GUS protein. Finally, a viral vector-based transformation method showed that MdHIR4 inhibited anthocyanin accumulation and fruit coloration in apple by modulating the expression of genes associated with anthocyanin biosynthesis.

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References

Lee J, He K, Stolc V, Lee H, Figueroa P, Gao Y . Analysis of transcription factor HY5 genomic binding sites revealed its hierarchical role in light regulation of development. Plant Cell. 2007; 19(3):731-49. PMC: 1867377. DOI: 10.1105/tpc.106.047688. View

Brueggemann J, Weisshaar B, Sagasser M . A WD40-repeat gene from Malus x domestica is a functional homologue of Arabidopsis thaliana TRANSPARENT TESTA GLABRA1. Plant Cell Rep. 2010; 29(3):285-94. DOI: 10.1007/s00299-010-0821-0. View

Shan X, Zhang Y, Peng W, Wang Z, Xie D . Molecular mechanism for jasmonate-induction of anthocyanin accumulation in Arabidopsis. J Exp Bot. 2009; 60(13):3849-60. DOI: 10.1093/jxb/erp223. View

Feller A, Machemer K, Braun E, Grotewold E . Evolutionary and comparative analysis of MYB and bHLH plant transcription factors. Plant J. 2011; 66(1):94-116. DOI: 10.1111/j.1365-313X.2010.04459.x. View

Nijtmans L, Artal S, Grivell L, Coates P . The mitochondrial PHB complex: roles in mitochondrial respiratory complex assembly, ageing and degenerative disease. Cell Mol Life Sci. 2002; 59(1):143-55. PMC: 11337490. DOI: 10.1007/s00018-002-8411-0. View

Fernandez-Calvo P, Chini A, Fernandez-Barbero G, Chico J, Gimenez-Ibanez S, Geerinck J . The Arabidopsis bHLH transcription factors MYC3 and MYC4 are targets of JAZ repressors and act additively with MYC2 in the activation of jasmonate responses. Plant Cell. 2011; 23(2):701-15. PMC: 3077776. DOI: 10.1105/tpc.110.080788. View

Zhou L, Cheung M, Zhang Q, Lei C, Zhang S, Sun S . A novel simple extracellular leucine-rich repeat (eLRR) domain protein from rice (OsLRR1) enters the endosomal pathway and interacts with the hypersensitive-induced reaction protein 1 (OsHIR1). Plant Cell Environ. 2009; 32(12):1804-20. DOI: 10.1111/j.1365-3040.2009.02039.x. View

Pauwels L, Goossens A . The JAZ proteins: a crucial interface in the jasmonate signaling cascade. Plant Cell. 2011; 23(9):3089-100. PMC: 3203442. DOI: 10.1105/tpc.111.089300. View

Dangl J, Dietrich R, Richberg M . Death Don't Have No Mercy: Cell Death Programs in Plant-Microbe Interactions. Plant Cell. 1996; 8(10):1793-1807. PMC: 161315. DOI: 10.1105/tpc.8.10.1793. View

10.

Umemura H, Otagaki S, Wada M, Kondo S, Matsumoto S . Expression and functional analysis of a novel MYB gene, MdMYB110a_JP, responsible for red flesh, not skin color in apple fruit. Planta. 2013; 238(1):65-76. DOI: 10.1007/s00425-013-1875-3. View

11.

Duan Y, Guo J, Shi X, Guan X, Liu F, Bai P . Wheat hypersensitive-induced reaction genes TaHIR1 and TaHIR3 are involved in response to stripe rust fungus infection and abiotic stresses. Plant Cell Rep. 2012; 32(2):273-83. DOI: 10.1007/s00299-012-1361-6. View

12.

Chagne D, Lin-Wang K, Espley R, Volz R, How N, Rouse S . An ancient duplication of apple MYB transcription factors is responsible for novel red fruit-flesh phenotypes. Plant Physiol. 2012; 161(1):225-39. PMC: 3532254. DOI: 10.1104/pp.112.206771. View

13.

Ban Y, Honda C, Hatsuyama Y, Igarashi M, Bessho H, Moriguchi T . Isolation and functional analysis of a MYB transcription factor gene that is a key regulator for the development of red coloration in apple skin. Plant Cell Physiol. 2007; 48(7):958-70. DOI: 10.1093/pcp/pcm066. View

14.

An X, Tian Y, Chen K, Wang X, Hao Y . The apple WD40 protein MdTTG1 interacts with bHLH but not MYB proteins to regulate anthocyanin accumulation. J Plant Physiol. 2012; 169(7):710-7. DOI: 10.1016/j.jplph.2012.01.015. View

15.

Browse J . Jasmonate: an oxylipin signal with many roles in plants. Vitam Horm. 2006; 72:431-56. DOI: 10.1016/S0083-6729(05)72012-4. View

16.

Loreti E, Povero G, Novi G, Solfanelli C, Alpi A, Perata P . Gibberellins, jasmonate and abscisic acid modulate the sucrose-induced expression of anthocyanin biosynthetic genes in Arabidopsis. New Phytol. 2008; 179(4):1004-1016. DOI: 10.1111/j.1469-8137.2008.02511.x. View

17.

Qi Y, Tsuda K, Nguyen L, Wang X, Lin J, Murphy A . Physical association of Arabidopsis hypersensitive induced reaction proteins (HIRs) with the immune receptor RPS2. J Biol Chem. 2011; 286(36):31297-307. PMC: 3173095. DOI: 10.1074/jbc.M110.211615. View

18.

Bi X, Zhang J, Chen C, Zhang D, Li P, Ma F . Anthocyanin contributes more to hydrogen peroxide scavenging than other phenolics in apple peel. Food Chem. 2014; 152:205-9. DOI: 10.1016/j.foodchem.2013.11.088. View

19.

Carbone F, Preuss A, de Vos R, DAmico E, Perrotta G, Bovy A . Developmental, genetic and environmental factors affect the expression of flavonoid genes, enzymes and metabolites in strawberry fruits. Plant Cell Environ. 2009; 32(8):1117-31. DOI: 10.1111/j.1365-3040.2009.01994.x. View

20.

Holton T, Cornish E . Genetics and Biochemistry of Anthocyanin Biosynthesis. Plant Cell. 1995; 7(7):1071-1083. PMC: 160913. DOI: 10.1105/tpc.7.7.1071. View