Abstract

Main conclusionTranscriptome and biochemical analyses suggested that, while suppression of multiple flavonoids and anthocyanins occurs at least partially at the transcriptional level, increased biosynthesis of non-jasmonate phyto-oxylipins is likely controlled non-transcriptionally.Methyl jasmonate (MeJA) produced in plants can mediate their response to environmental stresses. Exogenous application of MeJA has also shown to activate signaling pathways and induce phytoalexin accumulation in many plant species. To understand how pomegranate plants respond biochemically to environmental stresses, metabolite analysis was conducted in pomegranate leaves subjected to MeJA application and revealed unique changes in hydrolyzable tannins, flavonoids, and phyto-oxylipins. Additionally, transcriptome and real-time qPCR analyses of mock- and MeJA-treated pomegranate leaves identified differentially expressed metabolic genes and transcription factors that are potentially involved in the control of hydrolyzable tannin, flavonoid, and phyto-oxylipin pathways. Molecular, biochemical, and bioinformatic characterization of the only lipoxygenase with sustained, MeJA-induced expression showed that it is capable of oxidizing polyunsaturated fatty acids, though not located in the subcellular compartment where non-jasmonate (non-JA) phyto-oxylipins were produced. These results collectively suggested that while the broad suppression of flavonoids and anthocyanins is at least partially controlled at the transcriptional level, the induced biosynthesis of non-JA phyto-oxylipins is likely not regulated transcriptionally. Overall, a better understanding of how pomegranate leaves respond to environmental stresses will not only promote plant health and productivity, but also have an impact on human health as fruits produced by pomegranate plants are a rich source of nutritional compounds.

Highlights

  • When wounded or attacked by herbivores and pathogens, plants produce and emit methyl jasmonate (MeJA), which is perceived by non-wounded plant tissues and neighboring plants to activate defense response (Cheong and Choi 2003)

  • The biosynthesis of flavonoids and anthocyanins begins with the formation of naringenin chalcone from coumaroyl CoA and three molecules of malonyl CoA catalyzed by chalcone synthase (CHS) and the subsequent isomerization of naringenin chalcone to naringenin by chalcone isomerase (CHI)

  • Enhanced expression of PgUGT8423 and PgUGT84A24, which encode enzymes catalyzing the committed step of hydrolyzable tannins (HTs) biosynthesis, by Methyl jasmonate (MeJA) application further supports the role of HTs in stress response

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Summary

Introduction

When wounded or attacked by herbivores and pathogens, plants produce and emit methyl jasmonate (MeJA), which is perceived by non-wounded plant tissues and neighboring plants to activate defense response (Cheong and Choi 2003). Phyto-oxylipins are oxygenated fatty acids and derivatives that play a role in plant growth, development, stress response, and innate immunity (Wasternack and Feussner 2018). The initial step of phyto-oxylipin biosynthesis involves oxidation of polyunsaturated fatty acids (PUFAs) to fatty acid hydroperoxides (HPOs) by lipoxygenases (LOXs) (Andreou and Feussner 2009). Plant LOXs are grouped into two subfamilies according to their protein sequences; type I LOXs are highly homologous (> 75% similarity) and do not contain a signal peptide, whereas type II LOXs possess an overall low sequence similarity (< 35%) but all contain a chloroplast target peptide (Feussner and Wasternack 2002). Plant LOXs can be classified based on enzymatic activities; 9-LOXs and 13-LOXs target the C-9 and C-13 position of the fatty acid substrate, respectively (Feussner and Wasternack 2002). 13-hydroperoxy-linolenic acid (an HPO) produced from linolenic acid by 13-LOX can initiate a series of reactions to form jasmonic acid (JA), MeJA, and the bioactive JA-isoleucine conjugate

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