Participation of FaTRAB1 Transcription Factor in the Regulation of FaMADS1 Involved in ABA-Dependent Ripening of Strawberry Fruit

Abscisic acid (ABA) plays a crucial role in regulating the ripening of non-climacteric strawberry fruit. In the present study, ABA was confirmed to promote strawberry ripening and induce the down-regulation of FaMADS1. The transient silence of FaMADS1 in strawberries promoted fruit ripening and induced the content of anthocyanin and soluble pectin but reduced firmness and protopectin through a tobacco rattle virus-induced gene silencing technique. In parallel with the accelerated ripening, the genes were significantly induced in the transiently modified fruit, including anthocyanin-related PAL6, C4H, 4CL, DFR, and UFGT, softening-related PL and XTH, and aroma-related QR and AAT2. In addition, the interaction between FaMADS1 and ABA-related transcription factors was researched. Yeast one-hybrid analysis indicated that the FaMADS1 promoter could interact with FaABI5-5, FaTRAB1, and FaABI5. Furthermore, dual-luciferase assay suggested that FaTRAB1 could actively bind with the FaMADS1 promoter, resulting in the decreased expression of FaMADS1. In brief, these results suggest that the ABA-dependent ripening of strawberry fruit was probably inhibited through inhibiting FaMADS1 expression by the active binding of transcript FaTRAB1 with the FaMADS1 promoter.

[1]  Xiangbin Xu,et al.  Knockdown of Sly-miR160a using short tandem target mimic (STTM) enhanced expression of auxin signaling genes and delayed postharvest ripening of tomato fruit , 2023, Postharvest Biology and Technology.

[2]  L. Mao,et al.  ABA-mediated miR5290 promotes anthocyanin biosynthesis by inhibiting the expression of FaMADS1 in postharvest strawberry fruit , 2022, Postharvest Biology and Technology.

[3]  Zhongchi Liu,et al.  The MADS-box gene FveSEP3 plays essential roles in flower organogenesis and fruit development in woodland strawberry , 2021, Horticulture Research.

[4]  Zhaohui Xue,et al.  Abscisic acid and fruit ripening: Multifaceted analysis of the effect of abscisic acid on fleshy fruit ripening , 2021 .

[5]  L. Mao,et al.  ABA stimulates wound suberization through antagonizing the MYB4-mediated transcriptional repression of CYP86A1 and FAR in postharvest kiwifruit , 2021 .

[6]  Xiliang Qi,et al.  PaMADS7, a MADS-box transcription factor, regulates sweet cherry fruit ripening and softening. , 2020, Plant science : an international journal of experimental plant biology.

[7]  I. Ashikawa,et al.  TaABI5, a wheat homolog of Arabidopsis thaliana ABA insensitive 5, controls seed germination , 2020, Journal of Plant Research.

[8]  Wei Wei,et al.  Transcription factor FvTCP9 promotes strawberry fruit ripening by regulating the biosynthesis of abscisic acid and anthocyanins. , 2019, Plant physiology and biochemistry : PPB.

[9]  L. Mao,et al.  ABF2 and MYB transcription factors regulate feruloyl transferase FHT involved in ABA-mediated wound suberization of kiwifruit , 2019, Journal of experimental botany.

[10]  S. Masiero,et al.  Fruit ripening: the role of hormones, cell wall modifications, and their relationship with pathogens. , 2019, Journal of experimental botany.

[11]  T. Ying,et al.  Integrated analysis of high-throughput sequencing data shows abscisic acid-responsive genes and miRNAs in strawberry receptacle fruit ripening , 2019, Horticulture Research.

[12]  T. Ying,et al.  One novel strawberry MADS-box transcription factor FaMADS1a acts as a negative regulator in fruit ripening , 2018 .

[13]  Yuan-Yue Shen,et al.  A leu-rich repeat receptor-like protein kinase, FaRIPK1, interacts with the ABA receptor, FaABAR, to regulate fruit ripening in strawberry , 2017, Journal of experimental botany.

[14]  S. Bai,et al.  Dormancy-Associated MADS-Box (DAM) and the Abscisic Acid Pathway Regulate Pear Endodormancy Through a Feedback Mechanism , 2017, Plant & cell physiology.

[15]  P. Du,et al.  A FERONIA-Like Receptor Kinase Regulates Strawberry (Fragaria × ananassa) Fruit Ripening and Quality Formation , 2017, Front. Plant Sci..

[16]  C. Xiang,et al.  Arabidopsis MADS-Box Transcription Factor AGL21 Acts as Environmental Surveillance of Seed Germination by Regulating ABI5 Expression. , 2017, Molecular plant.

[17]  Min Liu,et al.  Effect of Exogenous Abscisic Acid and Methyl Jasmonate on Anthocyanin Composition, Fatty Acids, and Volatile Compounds of Cabernet Sauvignon (Vitis vinifera L.) Grape Berries , 2016, Molecules.

[18]  T. Ying,et al.  Developmental and stress regulation on expression of a novel miRNA, Fan-miR73, and its target ABI5 in strawberry , 2016, Scientific Reports.

[19]  E. Khayat,et al.  Banana MaMADS Transcription Factors Are Necessary for Fruit Ripening and Molecular Tools to Promote Shelf-Life and Food Security1[OPEN] , 2016, Plant Physiology.

[20]  I. Hwang,et al.  Abscisic acid: biosynthesis, inactivation, homoeostasis and signalling. , 2015, Essays in biochemistry.

[21]  Q. Xie,et al.  Precise protein post-translational modifications modulate ABI5 activity. , 2015, Trends in plant science.

[22]  W. Jia,et al.  SUCROSE NONFERMENTING1-RELATED PROTEIN KINASE2.6, an Ortholog of OPEN STOMATA1, Is a Negative Regulator of Strawberry Fruit Development and Ripening1[OPEN] , 2015, Plant Physiology.

[23]  Pei Chen,et al.  Effect of calcium on strawberry fruit flavonoid pathway gene expression and anthocyanin accumulation. , 2014, Plant physiology and biochemistry : PPB.

[24]  Maohua Wang,et al.  Potential role of pectate lyase and Ca(2+) in the increase in strawberry fruit firmness induced by short-term treatment with high-pressure CO2. , 2014, Journal of food science.

[25]  A. Fernie,et al.  The transcription factor AREB1 regulates primary metabolic pathways in tomato fruits , 2014, Journal of experimental botany.

[26]  S. Delrot,et al.  The Basic Leucine Zipper Transcription Factor ABSCISIC ACID RESPONSE ELEMENT-BINDING FACTOR2 Is an Important Transcriptional Regulator of Abscisic Acid-Dependent Grape Berry Ripening Processes1[W][OPEN] , 2013, Plant Physiology.

[27]  Tingting Dong,et al.  A Tomato MADS-Box Transcription Factor, SlMADS1, Acts as a Negative Regulator of Fruit Ripening1[C][W] , 2013, Plant Physiology.

[28]  G. Casadoro,et al.  A SHATTERPROOF-like gene controls ripening in non-climacteric strawberries, and auxin and abscisic acid antagonistically affect its expression , 2013, Journal of experimental botany.

[29]  Wenjing Lu,et al.  Cotton GhMKK1 Induces the Tolerance of Salt and Drought Stress, and Mediates Defence Responses to Pathogen Infection in Transgenic Nicotiana benthamiana , 2013, PloS one.

[30]  Vrani Ibarra-Junquera,et al.  Physical attributes and chemical composition of organic strawberry fruit (Fragaria x ananassa Duch, Cv. Albion) at six stages of ripening. , 2013, Food chemistry.

[31]  Yuan-Yue Shen,et al.  Type 2C protein phosphatase ABI1 is a negative regulator of strawberry fruit ripening , 2013, Journal of experimental botany.

[32]  Xue‐ren Yin,et al.  Ethylene-responsive transcription factors interact with promoters of ADH and PDC involved in persimmon (Diospyros kaki) fruit de-astringency , 2012, Journal of experimental botany.

[33]  Jun Cao The Pectin Lyases in Arabidopsis thaliana: Evolution, Selection and Expression Profiles , 2012, PloS one.

[34]  Ioannis Ganopoulos,et al.  The study of two barley Type I-like MADS-box genes as potential targets of epigenetic regulation during seed development , 2012, BMC Plant Biology.

[35]  W. Schwab,et al.  The fruit ripening-related gene FaAAT2 encodes an acyl transferase involved in strawberry aroma biogenesis. , 2012, Journal of experimental botany.

[36]  Yongzhong Liu,et al.  Comparison of cell wall metabolism in the pulp of three cultivars of 'Nanfeng' tangerine differing in mastication trait. , 2012, Journal of the science of food and agriculture.

[37]  Jie Ren,et al.  Transcriptional regulation of SlPYL, SlPP2C, and SlSnRK2 gene families encoding ABA signal core components during tomato fruit development and drought stress , 2011, Journal of experimental botany.

[38]  P. Civello,et al.  Cloning of FaPAL6 gene from strawberry fruit and characterization of its expression and enzymatic activity in two cultivars with different anthocyanin accumulation. , 2011, Plant science : an international journal of experimental plant biology.

[39]  Yuan-Yue Shen,et al.  Abscisic Acid Plays an Important Role in the Regulation of Strawberry Fruit Ripening1[W][OA] , 2011, Plant Physiology.

[40]  John P. Hammond,et al.  A SEPALLATA gene is involved in the development and ripening of strawberry (Fragaria×ananassa Duch.) fruit, a non-climacteric tissue* , 2010, Journal of experimental botany.

[41]  Da-Peng Zhang,et al.  The Mg-Chelatase H Subunit of Arabidopsis Antagonizes a Group of WRKY Transcription Repressors to Relieve ABA-Responsive Genes of Inhibition[W][OA] , 2010, Plant Cell.

[42]  S. Cao,et al.  Effect of BTH on anthocyanin content and activities of related enzymes in Strawberry after harvest. , 2010, Journal of agricultural and food chemistry.

[43]  Zhen Su,et al.  The Magnesium-Chelatase H Subunit Binds Abscisic Acid and Functions in Abscisic Acid Signaling: New Evidence in Arabidopsis1[W][OA] , 2009, Plant Physiology.

[44]  E. Grill,et al.  Regulators of PP2C Phosphatase Activity Function as Abscisic Acid Sensors , 2009, Science.

[45]  Wei-Hua Wu,et al.  A G Protein-Coupled Receptor Is a Plasma Membrane Receptor for the Plant Hormone Abscisic Acid , 2007, Science.

[46]  W. Schwab,et al.  RNAi-induced silencing of gene expression in strawberry fruit (Fragaria x ananassa) by agroinfiltration: a rapid assay for gene function analysis. , 2006, The Plant journal : for cell and molecular biology.

[47]  W. Schwab,et al.  Molecular characterization of a stable antisense chalcone synthase phenotype in strawberry (Fragaria x ananassa). , 2006, Journal of agricultural and food chemistry.

[48]  Hongliang Zhu,et al.  Virus-induced gene silencing in tomato fruit. , 2005, The Plant journal : for cell and molecular biology.

[49]  N. Goto-Yamamoto,et al.  STRUCTURE AND TRANSCRIPTION OF THREE CHALCONE SYNTHASE GENES OF GRAPEVINE (VITIS VINIFERA , 2003 .

[50]  Y. Kagaya,et al.  Abscisic Acid–Induced Transcription Is Mediated by Phosphorylation of an Abscisic Acid Response Element Binding Factor, TRAB1 Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.005272. , 2002, The Plant Cell Online.

[51]  T. Lynch,et al.  Regulation and Role of the Arabidopsis Abscisic Acid-Insensitive 5 Gene in Abscisic Acid, Sugar, and Stress Response1 , 2002, Plant Physiology.

[52]  N. Goto-Yamamoto,et al.  Structure and transcription of three chalcone synthase genes of grapevine (Vitis vinifera) , 2002 .

[53]  S. Dinesh-Kumar,et al.  Tobacco Rar1, EDS1 and NPR1/NIM1 like genes are required for N-mediated resistance to tobacco mosaic virus. , 2002, The Plant journal : for cell and molecular biology.

[54]  D. Brummell,et al.  Cell wall metabolism in fruit softening and quality and its manipulation in transgenic plants , 2001, Plant Molecular Biology.

[55]  M. Thomas,et al.  A cDNA from grapevine (Vitis vinifera L.), which shows homology to AGAMOUS and SHATTERPROOF, is not only expressed in flowers but also throughout berry development , 2001, Plant Molecular Biology.

[56]  E. Finnegan,et al.  The molecular basis of vernalization: the central role of FLOWERING LOCUS C (FLC). , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[57]  T. Hattori,et al.  A bZIP factor, TRAB1, interacts with VP1 and mediates abscisic acid-induced transcription. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[58]  W. Peacock,et al.  The FLF MADS Box Gene: A Repressor of Flowering in Arabidopsis Regulated by Vernalization and Methylation , 1999, Plant Cell.

[59]  I. Zabetakis,et al.  Strawberry Flavour: Analysis and Biosynthesis , 1997 .

[60]  Michael A. Jordan,et al.  The Composition of Strawberry Aroma Is Influenced by Cultivar, Maturity, and Storage , 1997 .

[61]  C. Sanz,et al.  Evolution of Strawberry Alcohol Acyltransferase Activity during Fruit Development and Storage , 1996 .

[62]  J. Cairney,et al.  A simple and efficient method for isolating RNA from pine trees , 1993, Plant Molecular Biology Reporter.

[63]  T. Ying,et al.  Involvement of abscisic acid in postharvest water-deficit stress associated with the accumulation of anthocyanins in strawberry fruit , 2016 .

[64]  Bart Nicolai,et al.  Optimization of HS SPME Fast GC-MS for High-Throughput Analysis of Strawberry Aroma , 2012, Food Analytical Methods.

[65]  G. Casadoro,et al.  Molecular analyses of MADS-box genes trace back to Gymnosperms the invention of fleshy fruits. , 2012, Molecular biology and evolution.

[66]  Kemal Hüsnü Can Başer,et al.  Quality characteristics of strawberry genotypes at different maturation stages , 2007 .

[67]  P. Andrews,et al.  Cell wall hydrolytic enzyme activity during development of nonclimacteric sweet cherry (Prunus avium L.) fruit , 1995 .