Comprehensive profiling of endogenous phytohormones and expression analysis of 1-aminocyclopropane-1-carboxylic acid synthase gene family during fruit development and ripening in octoploid strawberry (Fragaria× ananassa)

Authors: UPADHYAY, RAKESH - Purdue University; MOTYKA, VACLAV - Czech Academy Of Sciences; POKORNA, EVA - Czech Academy Of Sciences; DOBREV, PETRE - Czech Academy Of Sciences; LACEK, JOZEF - Czech Academy Of Sciences; Shao, Jonathan; Lewers, Kimberly; Mattoo, Autar

Submitted to: Plant Physiology and Biochemistry
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/16/2023
Publication Date: 1/18/2023
Citation: Upadhyay, R.K., Motyka, V., Pokorna, E., Dobrev, P.I., Lacek, J., Shao, J.Y., Lewers, K.S., Mattoo, A.K. 2023. Comprehensive profiling of endogenous phytohormones and expression analysis of 1-aminocyclopropane-1-carboxylic acid synthase gene family during fruit development and ripening in octoploid strawberry (Fragaria× ananassa). Plant Physiology and Biochemistry. 196:186-196. https://doi.org/10.1016/j.plaphy.2023.01.031.
DOI: https://doi.org/10.1016/j.plaphy.2023.01.031

Interpretive Summary: The ripening of fleshy fruits, both climacteric (tomato) and non-climacteric (strawberry), is the focus of interest in understanding the molecular regulation of the ripening process. Tomato ripening process is mainly regulated by the gaseous ethylene while strawberry ripening process is known to be governed by another hormone called abscisic acid. In recent years it has become clear that multiple processes are thought to be involved in the ripening of fruits. We used a non-climacteric octoploid strawberry (Fragaria×ananassa) and tomato to determine the processes of onset and regulation of fruit ripening. Determination of the molecular basis of ripening and quality attributes of the fruit such as nutritional quality, long keeping quality and disease resistance are fundamental for creating paths to avoid adverse climacteric conditions such as abiotic stress, to maintain nutritional quality of the fruit. In this study we identified novel phytohormone metabolites that are regulators of strawberry fruit ripening and developed an understanding of common and not so common factors that differentiate tomato ripening and that of strawberry. This research is of interest to strawberry and tomato breeders, scientists, plant physiologists and genetic experts.

Technical Abstract: The ripening of fleshy fruits, both climacteric and non-climacteric, is the focus of interest in understanding the molecular regulation of the ripening process. The non-climacteric octoploid strawberry (Fragaria×ananassa) was used as a model to study the regulation of fruit ripening. We used advanced high performance liquid chromatography electrospray tandem-mass spectrometry (HPLC-ESI-MS/MS) to profile 28 different endogenous phytohormones in strawberry, including auxins, cytokinins (CKs), abscisic acid (ABA), ethylene precursor 1-aminocyclopropane-1-carboxylic acid (ACC), jasmonates, and phenolic compounds salicylic acid (SA), benzoic acid (BzA) and phenylacetic acid (PAA), including their various metabolic forms, which have remained thus far largely unexplored. ABA, ACC and CK N6-('2-isopentenyl)adenine (iP) were found to be associated with ripening, and ABA catabolites such as 9-hydroxy-ABA and phaseic acid mimicked the pattern of climacteric decline in the turning phase of the ripening strawberry. The content of other CK forms except iP decreased as fruit ripened. The content of auxins indole-3-acetic acid (IAA) and oxo-IAA as well as jasmonates also decreased. Data obtained suggest that the transition and progression of strawberry fruit ripening are associated with N6-('2-isopentenyl)adenosine-5´-monophosphate (iPRMP) ' N6-('2-isopentenyl)adenosine (iPR) ' iP as the preferred CK metabolic pathway. In contrast to these data, the ethylene precursor ACC was found at higher levels, with its abundance increasing from the onset of ripening to the red ripe stage. Investigation of this ripening-specific ACC accumulation revealed the presence of a large ACC synthase (ACS) encoding gene family in octoploid strawberry that was previously unknown. Seventeen ACS genes were found to be differentially expressed in fruit tissues, with some showing high expression during strawberry fruit ripening. These data suggest a possible role of ACC, ABA, and iP in strawberry fruit ripening. Our study adds new dimensions to the existing knowledge on the interplay of different endogenous phytohormones in octoploid strawberry and paves the way for further investigation of their individual role(s) in fruit ripening.