Differential Triggering of the Phenylpropanoid Biosynthetic Pathway Key Genes Transcription upon Cold Stress and Viral Infection in Tomato Leaves

Plants develop a plethora of defense strategies during their acclimation and interactions with various environmental stresses. Secondary metabolites play a pivotal role in the processes during stress acclimation, therefore deciphering their relevant responses exchange the interpretation of the underlying molecular mechanisms that may contribute to improved adaptability and efficacy. In the current study, tomato plants were exposed to short-term cold stress (5 °C for 16 h) or inoculated (20 d) with either Cucumber Mosaic Virus (CMV) or Potato Virus Y (PVY). Responses were recorded via the assessments of leaf total phenolic (TP) content, total flavonoid (TF) levels, and phenylalanine ammonia-lyase (PAL) enzyme activity. The transcription of the gene families regulating the core phenylpropanoid biosynthetic pathway (PBP) at an early (PAL, cinnamic acid 4-hydroxylase, 4-coumarate-CoA ligase) or late (chalcone synthase and flavonol synthase) stage was also evaluated. The results showed that cold stress stimulated an increase in TP and TF contents, while PAL enzyme activity was also elevated compared to viral infection. Besides genes transcription of the enzymes involved in the core PBP was mostly induced by cold stress, whereas transcription of the genes regulating flavonoid biosynthesis was mainly triggered by viral infection. In conclusion, abiotic and biotic stressors induced differential regulation of the core PBP and flavonoid biosynthetic metabolism. Taking the above into consideration, our results highlight the complexity of tomato responses to diverse stimuli allowing for better elucidation of stress tolerance mechanisms at this crop.

[1]  T. Chatzistathis,et al.  Leaf Age-Dependent Effects of Boron Toxicity in Two Cucumis melo Varieties , 2021, Agronomy.

[2]  Yongcheng Chen,et al.  Low UVA intensity during cultivation improves the lettuce shelf-life, an effect that is not sustained at higher intensity , 2021 .

[3]  D. Šamec,et al.  The Role of Polyphenols in Abiotic Stress Response: The Influence of Molecular Structure , 2021, Plants.

[4]  N. Nikoloudakis,et al.  Leaf antioxidant machinery stimulation by Meloidogyne javanica infestation: A case study on Cucumis melo seedlings , 2021 .

[5]  G. Agati,et al.  Are Flavonoids Effective Antioxidants in Plants? Twenty Years of Our Investigation , 2020, Antioxidants.

[6]  A. García-Villaraco,et al.  Elicitation with Bacillus QV15 reveals a pivotal role of F3H on flavonoid metabolism improving adaptation to biotic stress in blackberry , 2020, PloS one.

[7]  G. Gheysen,et al.  Salicylic Acid Biosynthesis in Plants , 2020, Frontiers in Plant Science.

[8]  M. Fattahi,et al.  Cold stress changes antioxidant defense system, phenylpropanoid contents and expression of genes involved in their biosynthesis in Ocimum basilicum L. , 2020, Scientific Reports.

[9]  T. Ying,et al.  Effects of Exogenous Abscisic Acid on Bioactive Components and Antioxidant Capacity of Postharvest Tomato during Ripening , 2020, Molecules.

[10]  L. Xiaohong,et al.  Transcriptome analysis of Luffa cylindrica (L.) Roem response to infection with Cucumber mosaic virus (CMV). , 2020 .

[11]  N. Nikoloudakis,et al.  Polyamine Homeostasis in Tomato Biotic/Abiotic Stress Cross-Tolerance. , 2019, Gene.

[12]  Y. Rashad,et al.  Arbuscular Mycorrhizal Fungi Trigger Transcriptional Expression of Flavonoid and Chlorogenic Acid Biosynthetic Pathways Genes in Tomato against Tomato Mosaic Virus , 2019, Scientific Reports.

[13]  A. Rehman,et al.  Response of Phenylpropanoid Pathway and the Role of Polyphenols in Plants under Abiotic Stress , 2019, Molecules.

[14]  Niranjan Koirala,et al.  Total Phenolic Content, Flavonoid Content and Antioxidant Potential of Wild Vegetables from Western Nepal , 2019, Plants.

[15]  A. Giri,et al.  Structural, functional and evolutionary diversity of 4-coumarate-CoA ligase in plants , 2018, Planta.

[16]  K. Zandi,et al.  Flavonoids: promising natural compounds against viral infections , 2017, Archives of Virology.

[17]  Sheela Chandra,et al.  Flavonoids: an overview , 2016, Journal of Nutritional Science.

[18]  Yongping Cai,et al.  Systematic Analysis of the 4-Coumarate:Coenzyme A Ligase (4CL) Related Genes and Expression Profiling during Fruit Development in the Chinese Pear , 2016, Genes.

[19]  A. Fernie,et al.  Flavonoids are determinants of freezing tolerance and cold acclimation in Arabidopsis thaliana , 2016, Scientific Reports.

[20]  W. Weckwerth,et al.  Primary Metabolism, Phenylpropanoids and Antioxidant Pathways Are Regulated in Potato as a Response to Potato virus Y Infection , 2016, PloS one.

[21]  C. Chapple,et al.  Four Isoforms of Arabidopsis 4-Coumarate:CoA Ligase Have Overlapping yet Distinct Roles in Phenylpropanoid Metabolism1[OPEN] , 2015, Plant Physiology.

[22]  R. Amarowicz,et al.  The effects of cold stress on the phenolic compounds and antioxidant capacity of grapevine (Vitis vinifera L.) leaves. , 2015, Journal of plant physiology.

[23]  T. Candresse,et al.  A novel grapevine badnavirus is associated with the Roditis leaf discoloration disease. , 2015, Virus research.

[24]  A. Fernie,et al.  Virus-Induced Alterations in Primary Metabolism Modulate Susceptibility to Tobacco rattle virus in Arabidopsis1[C][W] , 2014, Plant Physiology.

[25]  Y. Haviv,et al.  Comparative metabolomics and transcriptomics of plant response to Tomato yellow leaf curl virus infection in resistant and susceptible tomato cultivars , 2014, Metabolomics.

[26]  Jun Yu,et al.  Predicting the Function of 4-Coumarate:CoA Ligase (LJ4CL1) in Lonicera japonica , 2014, International journal of molecular sciences.

[27]  A. Pandey,et al.  Chemistry and Biological Activities of Flavonoids: An Overview , 2013, TheScientificWorldJournal.

[28]  Takayuki Tohge,et al.  The evolution of phenylpropanoid metabolism in the green lineage , 2013, Critical reviews in biochemistry and molecular biology.

[29]  Giovanni Agati,et al.  Flavonoids as antioxidants in plants: location and functional significance. , 2012, Plant science : an international journal of experimental plant biology.

[30]  P. Urwin,et al.  The interaction of plant biotic and abiotic stresses: from genes to the field. , 2012, Journal of experimental botany.

[31]  F. Ferrini,et al.  Stress-induced flavonoid biosynthesis and the antioxidant machinery of plants , 2011, Plant signaling & behavior.

[32]  James F Harbertson,et al.  Modulation of flavonoid biosynthetic pathway genes and anthocyanins due to virus infection in grapevine (Vitis vinifera L.) leaves , 2010, BMC Plant Biology.

[33]  U. Niinemets Mild versus severe stress and BVOCs: thresholds, priming and consequences. , 2010, Trends in plant science.

[34]  T. Vogt Phenylpropanoid biosynthesis. , 2010, Molecular plant.

[35]  Jean-Michel Claverie,et al.  Phylogeny.fr: robust phylogenetic analysis for the non-specialist , 2008, Nucleic Acids Res..

[36]  Andrew J Lamb,et al.  Antimicrobial activity of flavonoids , 2005, International Journal of Antimicrobial Agents.

[37]  L. Ferretti,et al.  DISTRIBUTION OF OLIVE TREE VIRUSES IN ITALY AS REVEALED BY ONE-STEP RT-PCR , 2005 .

[38]  N. Katis,et al.  Generic detection and differentiation of tobamoviruses by a spot nested RT-PCR-RFLP using dI-containing primers along with homologous dG-containing primers. , 2004, Journal of virological methods.

[39]  Dietmar Schomburg,et al.  The substrate specificity-determining amino acid code of 4-coumarate:CoA ligase , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[40]  R. Lamuela-Raventós,et al.  Analysis of total phenols and other oxidation substrates and antioxidants by means of Folin-Ciocalteu reagent , 1999 .

[41]  Chung-Jui Tsai,et al.  Compartmentalized expression of two structurally and functionally distinct 4-coumarate:CoA ligase genes in aspen (Populus tremuloides). , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[42]  R. Dixon,et al.  Stress-Induced Phenylpropanoid Metabolism. , 1995, The Plant cell.

[43]  L. Pellegrini,et al.  Phenylalanine Ammonia-Lyase in Tobacco (Molecular Cloning and Gene Expression during the Hypersensitive Reaction to Tobacco Mosaic Virus and the Response to a Fungal Elicitor) , 1994, Plant physiology.

[44]  I. Barker,et al.  The detection of tomato spotted wilt virus using the polymerase chain reaction. , 1994, Journal of virological methods.

[45]  J. Selway Antiviral activity of flavones and flavans. , 1986, Progress in clinical and biological research.