Brassinosteroid Regulates 3-Hydroxy-3-methylglutaryl CoA Reductase to Promote Grape Fruit Development.

Brassinosteroids (BRs) are known to regulate plant growth and development. However, only little is known about their mechanism in the regulation of berry development in grapes. This study demonstrates that BR treatment enhances the accumulation of fruit sugar components, reduces the content of organic acids (e.g., tartaric acid), promotes coloration, and increases the anthocyanin content in grape berries at the onset of the veraison, half veraison, and full veraison stages at the rate of 0.0998, 0.0560, and 0.0281 mg·g-1, respectively. In addition, BR treatment was also found to accelerate the biosynthesis of terpenoid aroma components, such as α-pinene, d-limonene, and γ-terpinene, which influence the aromatic composition of grapes. BRs can negatively regulate the expression of VvHMGR, a key gene involved in the mevalonate (MVA) pathway, and reduce the activity of 3-hydroxy-3-methylglutaryl CoA reductase (HMGR). Inhibiting the expression of HMGR promoted the accumulation of anthocyanins and fruit coloration. Meanwhile, after the inhibition, the contents of auxin indole-3-acetic acid (IAA), abscisic acid (ABA), and brassinosteroid (BR) increased, while gibberellin (GA3) and zeatin riboside (ZR) decreased, and its aromatic composition also changed. Therefore, it may be concluded that BRs inhibited HMGR activity and cooperated with VvHMGR to regulate the formation of color, aroma, and other quality characteristics in fruits.

[1]  H. Jia,et al.  Effect of methylation level on grape fruit development process. , 2020, Journal of agricultural and food chemistry.

[2]  Songtao Jiu,et al.  Integrated metatranscriptome and transcriptome reveals the microbial community composition and physiological function of xylem sap on grapevine during bleeding period , 2019, Genes & Genomics.

[3]  M. M. Dawuda,et al.  Anthocyanin accumulation correlates with hormones in the fruit skin of ‘Red Delicious’ and its four generation bud sport mutants , 2018, BMC Plant Biology.

[4]  Jiangfei Meng,et al.  Exogenous 24-Epibrassinolide alleviates oxidative damage from copper stress in grape (Vitis vinifera L.) cuttings. , 2018, Plant physiology and biochemistry : PPB.

[5]  Songtao Jiu,et al.  Changes of Anthocyanin Component Biosynthesis in 'Summer Black' Grape Berries after the Red Flesh Mutation Occurred. , 2018, Journal of agricultural and food chemistry.

[6]  Xiaofeng Wang,et al.  Enhancing Brassinosteroid Signaling via Overexpression of Tomato (Solanum lycopersicum) SlBRI1 Improves Major Agronomic Traits , 2017, Front. Plant Sci..

[7]  Xunzhong Zhang,et al.  Physiological Mechanism of Enhancing Salt Stress Tolerance of Perennial Ryegrass by 24-Epibrassinolide , 2017, Front. Plant Sci..

[8]  Yiting Shi,et al.  BZR1 Positively Regulates Freezing Tolerance via CBF-Dependent and CBF-Independent Pathways in Arabidopsis. , 2017, Molecular plant.

[9]  P. Trivedi,et al.  Genes encoding members of 3-hydroxy-3-methylglutaryl coenzyme A reductase (HMGR) gene family from Azadirachta indica and correlation with azadirachtin biosynthesis , 2017, Acta Physiologiae Plantarum.

[10]  J. Chai,et al.  Q&A: what are brassinosteroids and how do they act in plants? , 2016, BMC Biology.

[11]  Jihua Yu,et al.  Transcriptome Analysis of Pepper (Capsicum annuum) Revealed a Role of 24-Epibrassinolide in Response to Chilling , 2016, Front. Plant Sci..

[12]  T. A. Khan,et al.  Interaction of epibrassinolide and selenium ameliorates the excess copper in Brassica juncea through altered proline metabolism and antioxidants. , 2016, Ecotoxicology and environmental safety.

[13]  A. Bajguz,et al.  Brassinosteroids and Response of Plants to Heavy Metals Action , 2016, Front. Plant Sci..

[14]  Jie Zhou,et al.  Overexpression of a brassinosteroid biosynthetic gene Dwarf enhances photosynthetic capacity through activation of Calvin cycle enzymes in tomato , 2016, BMC Plant Biology.

[15]  T. Zhu,et al.  Ethylene is Involved in Brassinosteroids Induced Alternative Respiratory Pathway in Cucumber (Cucumis sativus L.) Seedlings Response to Abiotic Stress , 2015, Front. Plant Sci..

[16]  S. Clouse.  A History of Brassinosteroid Research from 1970 through 2005: Thirty-Five Years of Phytochemistry, Physiology, Genes, and Mutants , 2015, Journal of Plant Growth Regulation.

[17]  C. López-Iglesias,et al.  Proliferation and Morphogenesis of the Endoplasmic Reticulum Driven by the Membrane Domain of 3-Hydroxy-3-Methylglutaryl Coenzyme A Reductase in Plant Cells1[OPEN] , 2015, Plant Physiology.

[18]  N. B. Talaat,et al.  Alleviation of drought-induced oxidative stress in maize (Zea mays L.) plants by dual application of 24-epibrassinolide and spermine , 2015 .

[19]  A. Fortes,et al.  Complex Interplay of Hormonal Signals during Grape Berry Ripening , 2015, Molecules.

[20]  Zhi-Yong Wang,et al.  Spatiotemporal Brassinosteroid Signaling and Antagonism with Auxin Pattern Stem Cell Dynamics in Arabidopsis Roots , 2015, Current Biology.

[21]  Aditi Gupta,et al.  Interaction between Glucose and Brassinosteroid during the Regulation of Lateral Root Development in Arabidopsis1 , 2015, Plant Physiology.

[22]  T. Zhu,et al.  Effects of brassinosteroids on quality attributes and ethylene synthesis in postharvest tomato fruit , 2015 .

[23]  S. Savaldi-Goldstein,et al.  Growth control: brassinosteroid activity gets context. , 2015, Journal of experimental botany.

[24]  G. Wang,et al.  Brassinosteroids alleviate high-temperature injury in Ficus concinna seedlings via maintaining higher antioxidant defence and glyoxalase systems , 2015, AoB PLANTS.

[25]  Xiang Gao,et al.  Application of exogenous 24-epibrassinolide enhances proanthocyanidin biosynthesis in Vitis vinifera ‘Cabernet Sauvignon’ berry skin , 2014, Plant Growth Regulation.

[26]  M. Chye,et al.  Transgenic Tobacco Overexpressing Brassica juncea HMG-CoA Synthase 1 Shows Increased Plant Growth, Pod Size and Seed Yield , 2014, PloS one.

[27]  Deok-Chun Yang,et al.  Functional Analysis of 3-Hydroxy-3-Methylglutaryl Coenzyme A Reductase Encoding Genes in Triterpene Saponin-Producing Ginseng1[C][W] , 2014, Plant Physiology.

[28]  M. Zhang,et al.  Ectopic expression of a BZR1-1D transcription factor in brassinosteroid signalling enhances carotenoid accumulation and fruit quality attributes in tomato. , 2014, Plant biotechnology journal.

[29]  Xiang Gao,et al.  Regulating the secondary metabolism in grape berry using exogenous 24-epibrassinolide for enhanced phenolics content and antioxidant capacity. , 2013, Food chemistry.

[30]  J. Dinneny,et al.  A Spatio-Temporal Understanding of Growth Regulation during the Salt Stress Response in Arabidopsis[W] , 2013, Plant Cell.

[31]  R. Creelman,et al.  Overexpression of 3-hydroxy-3-methylglutaryl coenzyme A reductase in Parthenium argentatum (guayule) , 2013 .

[32]  Zhixiang Chen,et al.  Silencing of tomato RBOH1 and MPK2 abolishes brassinosteroid-induced H₂O₂ generation and stress tolerance. , 2013, Plant, cell & environment.

[33]  K. Shinozaki,et al.  Benefits of brassinosteroid crosstalk. , 2012, Trends in plant science.

[34]  A. Eneji,et al.  Mechanism of phytohormone involvement in feedback regulation of cotton leaf senescence induced by potassium deficiency , 2012, Journal of experimental botany.

[35]  Morteza Soleimani Aghdam,et al.  Impact of postharvest brassinosteroids treatment on PAL activity in tomato fruit in response to chilling stress , 2012 .

[36]  Yuan-Yue Shen,et al.  Brassinosteroid is involved in strawberry fruit ripening , 2012, Plant Growth Regulation.

[37]  Parul Gupta,et al.  Cloning and functional characterization of 3-hydroxy-3-methylglutaryl coenzyme A reductase gene from Withania somnifera: an important medicinal plant , 2012, Protoplasma.

[38]  R. Sangwan,et al.  Withanolide biosynthesis recruits both mevalonate and DOXP pathways of isoprenogenesis in Ashwagandha Withania somnifera L. (Dunal) , 2012, Plant Cell Reports.

[39]  Baohua Cao,et al.  Brassinolide enhances cold stress tolerance of fruit by regulating plasma membrane proteins and lipids , 2012, Amino Acids.

[40]  Shilin Chen,et al.  Genome-wide identification and characterization of novel genes involved in terpenoid biosynthesis in Salvia miltiorrhiza , 2022 .

[41]  Y. J. Liu,et al.  Effect of 24-epibrassinolide on drought stress-induced changes in Chorispora bungeana , 2011, Biologia Plantarum.

[42]  J. B. Reid,et al.  Role of Brassinosteroids, Ethylene, Abscisic Acid, and Indole-3-Acetic Acid in Mango Fruit Ripening , 2011, Journal of Plant Growth Regulation.

[43]  A. Ferrer,et al.  Modulation of plant HMG-CoA reductase by protein phosphatase 2A , 2011, Plant signaling & behavior.

[44]  A. Ferrer,et al.  Multilevel Control of Arabidopsis 3-Hydroxy-3-Methylglutaryl Coenzyme A Reductase by Protein Phosphatase 2A[W] , 2011, Plant Cell.

[45]  S. R. Guo,et al.  Role of brassinosteroids on horticultural crops , 2011 .

[46]  G. Qin,et al.  Effects of brassinosteroids on postharvest disease and senescence of jujube fruit in storage , 2010 .

[47]  X. Hua,et al.  Arabidopsis Brassinosteroid Mutants det2-1 and bin2-1 Display Altered Salt Tolerance , 2010, Journal of Plant Growth Regulation.

[48]  D. Shibata,et al.  Molecular and genetic characterization of transgenic tomato expressing 3-hydroxy-3-methylglutaryl coenzyme A reductase , 2007 .

[49]  Gregory M Symons,et al.  Grapes on Steroids. Brassinosteroids Are Involved in Grape Berry Ripening1 , 2005, Plant Physiology.

[50]  P. Fraser,et al.  Metabolic engineering of the mevalonate and non-mevalonate isopentenyl diphosphate-forming pathways for the production of health-promoting isoprenoids in tomato. , 2004, Plant biotechnology journal.

[51]  V. Rodwell,et al.  The 3-hydroxy-3-methylglutaryl coenzyme-A (HMG-CoA) reductases , 2004, Genome Biology.

[52]  H. Ezura,et al.  Detection of 3-hydroxy-3-methylglutaryl-coenzyme A reductase protein Cm-HMGR during fruit development in melon (Cucumis melo L.) , 2002, Theoretical and Applied Genetics.

[53]  D. Crowell,et al.  Inhibition of growth of cultured tobacco cells at low concentrations of lovastatin is reversed by cytokinin. , 1992, Plant physiology.

[54]  R. Bostock,et al.  Differential induction and suppression of potato 3-hydroxy-3-methylglutaryl coenzyme A reductase genes in response to Phytophthora infestans and to its elicitor arachidonic acid. , 1992, The Plant cell.

[55]  I. Tsuritani,et al.  Effect of auxin on the metabolism of mevalonic acid in suspension-cultured carrot cells , 1983 .