FaPAO5 regulates Spm/Spd levels as a signaling during strawberry fruit ripening

Abstract

Polyamines are important for non-climacteric fruit ripening according to an analysis of the model plant strawberry. However, the molecular mechanism underlying the polyamine accumulation during ripening has not been fully elucidated. In this study, an examination of our proteome data related to strawberry fruit ripening revealed a putative polyamine oxidase 5, FaPAO5, which was localized in the cytoplasm and nucleus. Additionally, FaPAO5 expression levels as well as the abundance of the encoded protein continually decreased during ripening. Inhibiting FaPAO5 expression by RNAi promoted Spd, Spm, and ABA accumulation while inhibited H 2 O 2 production, which ultimately enhanced ripening as evidenced by the ripening-related events and corresponding gene expression changes. The opposite effects were observed in FaPAO5-overexpressing transgenic fruits. Analyses of the binding affinity and enzymatic activity of FaPAO5 with Spm, Spd, and Put uncovered a special role for FaPAO5 in the terminal catabolism of Spm and Spd, with a K d of 0.21 and 0.29 µM, respectively. Moreover, FaPAO5 expression was inhibited by ABA and promoted by Spd and Spm. Furthermore, the RNA-seq analysis of RNAi and control fruits via differentially expressed genes (DEGs) indicated the six most enriched pathways among the differentially expressed genes were related to sugar, abscisic acid, ethylene, auxin, gibberellin, and Ca 2+ . Among four putative PAO genes in the strawberry genome,only FaPAO5 was confirmed to influence fruit ripening. In conclusion, FaPAO5 is a negative regulator of strawberry fruit ripening and modulates Spm/Spd levels as a signaling event, in which ABA plays a central role.

The Physiological and Molecular Mechanism of Abscisic Acid in Regulation of Fleshy Fruit Ripening

“…During strawberry fruit ripening, polyamines (PAs), especially spermine, interact with ABA, IAA, and ethylene in a coordinated manner ( Guo et al, 2018 ). Increased transcription of NCED3 , key to ABA production, at the onset of strawberry fruit ripening facilitates rapid accumulation of ABA, which inhibits transcription of FaPAO5 ( polyamine oxidase5 ), key to PA degradation, leading to accumulation of spermine and spermidine ( Mo et al, 2020 ). Interestingly, the increase in spermine and spermidine contents triggers expression of SAMDC (SAM decar boxylase), SPDS (spermidine synthase), and SPMS (spermine synthase) genes, key to PA biosynthesis, further accelerating spermine and spermidine accumulation and ripening, suggesting that FaPAO5 regulates spermine and spermidine levels in response to ABA signaling during strawberry fruit ripening ( Mo et al, 2020 ).…”

“…The promotion of grape berry ripening by ABA, ethylene, and brassinosteroids, and ripening inhibition by IAA, jasmonic acid, GAs, cytokinins, and PAs reveal complex interactions among signals ( Fortes et al, 2015 ). Notably, polyamines regulate strawberry fruit ripening by ABA, auxin and ethylene ( Guo et al, 2018 ), while FaPAO5 regulates Spm/Spd levels as a signaling during strawberry fruit ripening by integrating multiple signals including Ca 2+ and GAs ( Mo et al, 2020 ).…”

Update on the Roles of Polyamines in Fleshy Fruit Ripening, Senescence, and Quality

“…In the past decades, much progress has been made toward a better understanding of the roles of PAs in various fleshy fruits, such as avocado ( Persea americana ; Kushad et al, 1988 ), tomato ( Dibble et al, 1988 ; Mehta et al, 2002 ; Mattoo et al, 2006 , 2007 , 2010 ), eggplant ( Solanum melongena ; Rodriguez et al, 1999 ), muskmelon ( Cucumis melo ; Lester, 2000 ), peach ( Prunus persica ; Bregoli et al, 2002 ), damson plum ( Prunus salicina ; de Dios et al, 2006 ), olive ( Canarium album ; Parra-Lobato and Gomez-Jimenez, 2011 ), apricot ( Prunus armeniaca ; Koushesh saba et al, 2012 ), apple ( Malus sylvestris var. domestica ; Kitashiba et al, 2005 ), loquat ( Dimocarpus longgana Lour; Jiang et al, 2015 ), grape ( Vitis vinifera ; Fortes et al, 2015 ), raspberry ( Rubus idaeus ; Simpson et al, 2017 ), and strawberry ( Guo et al, 2018 ; Mo et al, 2020 ).…”

“…In comparison to the many advances describing the roles of PAs in climacteric fruits over many years, it is only recently that breakthroughs as in grape and strawberry have been made toward elucidating whether and how PAs participate in non-climacteric fruit ripening, senescence, and quality ( Agudelo-Romero et al, 2013 , 2014 ; Fortes et al, 2015 ; Guo et al, 2018 ; Mo et al, 2020 ).…”

“…Much progress has been made toward elucidating the PA biosynthetic pathway and PA metabolism in climacteric fruits, largely using tomato as a model ( Kushad et al, 1988 ; Rastogi and Davies, 1990 , 1991 ; Mehta et al, 2002 ; Nambeesan et al, 2010 ; Kolotilin et al, 2011 ; Neily et al, 2011 ; Pandey et al, 2015 ; Tsaniklidis et al, 2016 ; Liu et al, 2018 ). Encouragingly, the biosynthesis and metabolism of PAs in non-climacteric fruits have also been recently deciphered, using strawberry as the model plant ( Guo et al, 2018 ; Mo et al, 2020 ).…”