Transition from development to ripening of tomato fruit impacts abundance of endogenous phytohormones and their pathway metabolites

Authors: UPADHYAY, RAKESH - US Department Of Agriculture (USDA); MOTYKA, VACLAV - Academy Of Sciences Of The Czech Republic (ASCR); POKORNA, EVA - Academy Of Sciences Of The Czech Republic (ASCR); ROBERTA, FILEPOVÁ - Academy Of Sciences Of The Czech Republic (ASCR); DOBREV, PETRE - Purdue University; HANDA, AVTAR - Purdue University; Mattoo, Autar

Submitted to: Plant Growth Regulation
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/25/2024
Publication Date: 6/13/2024
Citation: Upadhyay, R.K., Motyka, V., Pokorna, E., Roberta, F., Dobrev, P.I., Handa, A.K., Mattoo, A.K. 2024. Transition from development to ripening of tomato fruit impacts abundance of endogenous phytohormones and their pathway metabolites. Plant Growth Regulation. https://doi.org/10.1007/s10725-024-01165-7.
DOI: https://doi.org/10.1007/s10725-024-01165-7

Interpretive Summary: Nutritionally rich and climate resilient crops are needed to secure high quality, nonperishable vegetables and fruits for the growing population. Sustainable agriculture of horticulture crops is therefore an important way to achieve this goal. In tomato, various aspects of fruit quality are tightly associated with its ripening process and is mainly governed by the hormone ethylene and other factors, however, the knowledge of other phytohormone metabolites is scarce. The phytohormones involved in regulating such traits are therefore of paramount importance. A comprehensive profiling of phytohormones is therefore necessary to shed light on novel hormones/metabolites in order to identify new pathways and their regulatory gene networks. The scientific understanding of fruit ripening process is also necessary to understand the molecular basis of ripening to enhance nutritional quality, long keeping quality and disease resistance of horticultural crops. Therefore, the focus of the present study was to identify new phytohormone metabolites that regulate ripening process of fruits and vegetables. This research is of interest to fruit crop breeders, scientists, plant physiologists, and genetic experts.

Technical Abstract: Molecular regulation of fruit ripening is fundamental for sustainable production of quality fruits with desired traits. Eth¬ylene and abscisic acid (ABA) are two of the most studied plant hormones during fruit development, onset, and progres¬sion 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 com¬pounds 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-('2-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 develop¬ment and ripening of fleshy tomato fruit.