A comprehensive endogenous phytohormone metabolite landscape identifies new metabolites associated with tomato fruit
Upadhyay R.K., Motyka V., Pokorná E., Filepová R, Dobrev P.I., Handa A.K., Mattoo A.K.
PLANT GROWTH REGULATION 104: 343-357, 2024
Keywords: Phytohormone, cytokinin, auxin, fruit, ripening, tomato
Abstract: Molecular regulation of fruit ripening is fundamental for sustainable production of quality fruits with desired traits. Ethylene and abscisic acid (ABA) are two of the most studied plant hormones during fruit development, onset, and progression of fruit ripening, while the abundance and role(s) of other phytohormones have remained elusive. Here, we used high-performance liquid chromatography-tandem mass spectrometry (LC-MS/MS) to quantify endogenous concentrations of numerous plant hormones, namely cytokinins (CKs), auxins, gibberellins, jasmonates, ABA and salicylic acid (SA), as well as their pathway metabolites during tomato fruit development and ripening. Changes in the levels of 47 compounds including active phytohormones and their derivatives during fruit development (stages Dev1, Dev2 and Dev3) and ripening (stages mature green, breaker, breaker + 3 d and breaker + 8 days) of tomato fruit were identified. Quantitative multivariant analyses of the phytohormones and their related compounds involving the seven analyzed stages showed their differential accumulation during fruit development and ripening. Early developmental stage (Dev1) of cell number proliferation was associated with auxins (IAA-GE, IAA-Glu, OxIAA-GE, OxIAA, and OxIAA-Asp), trans-zeatin (tZ)-, dihydrozeatin (DZ)- and N6-(Δ2-isopentenyl) adenine (iP)-type CKs (tZ7G, tZ9G, tZRMP, tZOG, DZOG, iP7G, iP9G), jasmonic acid (JA)-isoleucine, and gibberellin GA29. The cell expansion phase, Dev2, was found associated with auxins IAA-Asp and I3A, gibberellins GA19 and GA20, JA, SA and phenylacetic acid. Abundance of ABA and benzoic acid at the maturation phase (Dev3), mature green and breaker stages of fruit development were apparent. At the fruit ripening phase (BR + 3 and BR + 8) accumulation of iP-, cis-zeatin (cZ)-, tZ-, DZ-type CKs (iP, iPR, iPRMP, cZR, cZ7G, cZROG, cZRMP, tZR, tZROG, DZR, DZRMP) and CK methylthioderivatives (MeS-Z, MeS-ZR), auxin IAM, and jasmonates DiH-JA and JA-Me was apparent. Notably, the mevalonate CK pathway cZRMP→cZR→cZ was found to be the dominant pathway during fruit ripening, which contrasts with the known CK abundances in non-climacteric fruits. Taken together, these results provide a map of the differential accumulation of phytohormones and their metabolites during the development and ripening of fleshy tomato fruit.
DOI: 10.1007/s10725-024-01165-7
Fulltext: contact IEB authors
IEB authors: Petre I. Dobrev, Roberta Filepová, Václav Motyka, Eva Pokorná
PLANT GROWTH REGULATION 104: 343-357, 2024
Keywords: Phytohormone, cytokinin, auxin, fruit, ripening, tomato
Abstract: Molecular regulation of fruit ripening is fundamental for sustainable production of quality fruits with desired traits. Ethylene and abscisic acid (ABA) are two of the most studied plant hormones during fruit development, onset, and progression of fruit ripening, while the abundance and role(s) of other phytohormones have remained elusive. Here, we used high-performance liquid chromatography-tandem mass spectrometry (LC-MS/MS) to quantify endogenous concentrations of numerous plant hormones, namely cytokinins (CKs), auxins, gibberellins, jasmonates, ABA and salicylic acid (SA), as well as their pathway metabolites during tomato fruit development and ripening. Changes in the levels of 47 compounds including active phytohormones and their derivatives during fruit development (stages Dev1, Dev2 and Dev3) and ripening (stages mature green, breaker, breaker + 3 d and breaker + 8 days) of tomato fruit were identified. Quantitative multivariant analyses of the phytohormones and their related compounds involving the seven analyzed stages showed their differential accumulation during fruit development and ripening. Early developmental stage (Dev1) of cell number proliferation was associated with auxins (IAA-GE, IAA-Glu, OxIAA-GE, OxIAA, and OxIAA-Asp), trans-zeatin (tZ)-, dihydrozeatin (DZ)- and N6-(Δ2-isopentenyl) adenine (iP)-type CKs (tZ7G, tZ9G, tZRMP, tZOG, DZOG, iP7G, iP9G), jasmonic acid (JA)-isoleucine, and gibberellin GA29. The cell expansion phase, Dev2, was found associated with auxins IAA-Asp and I3A, gibberellins GA19 and GA20, JA, SA and phenylacetic acid. Abundance of ABA and benzoic acid at the maturation phase (Dev3), mature green and breaker stages of fruit development were apparent. At the fruit ripening phase (BR + 3 and BR + 8) accumulation of iP-, cis-zeatin (cZ)-, tZ-, DZ-type CKs (iP, iPR, iPRMP, cZR, cZ7G, cZROG, cZRMP, tZR, tZROG, DZR, DZRMP) and CK methylthioderivatives (MeS-Z, MeS-ZR), auxin IAM, and jasmonates DiH-JA and JA-Me was apparent. Notably, the mevalonate CK pathway cZRMP→cZR→cZ was found to be the dominant pathway during fruit ripening, which contrasts with the known CK abundances in non-climacteric fruits. Taken together, these results provide a map of the differential accumulation of phytohormones and their metabolites during the development and ripening of fleshy tomato fruit.
DOI: 10.1007/s10725-024-01165-7
Fulltext: contact IEB authors
IEB authors: Petre I. Dobrev, Roberta Filepová, Václav Motyka, Eva Pokorná