Tomato transcriptome and mutant analyses suggest a role for plant stress hormones in the interaction between fruit and Botrytis cinerea

Abstract

Fruit–pathogen interactions are a valuable biological system to study the role of plant development in the transition from resistance to susceptibility. In general, unripe fruit are resistant to pathogen infection but become increasingly more susceptible as they ripen. During ripening, fruit undergo significant physiological and biochemical changes that are coordinated by complex regulatory and hormonal signaling networks. The interplay between multiple plant stress hormones in the interaction between plant vegetative tissues and microbial pathogens has been documented extensively, but the relevance of these hormones during infections of fruit is unclear. In this work, we analyzed a transcriptome study of tomato fruit infected with Botrytis cinerea in order to profile the expression of genes for the biosynthesis, modification and signal transduction of ethylene (ET), salicylic acid (SA), jasmonic acid (JA), and abscisic acid (ABA), hormones that may be not only involved in ripening, but also in fruit interactions with pathogens. The changes in relative expression of key genes during infection and assays of susceptibility of fruit with impaired synthesis or perception of these hormones were used to formulate hypotheses regarding the involvement of these regulators in the outcome of the tomato fruit–B. cinerea interaction.

Developmental and metabolic plasticity of white-skinned grape berries in response to Botrytis cinerea during noble rot

“…Total RNA was obtained from 2 g of ground tissue (skin and pulp) using the protocol described by Blanco-Ulate et al (2013b). The concentration and purity of the RNA were measured using the NanoDrop 2000c Spectrophotometer (Thermo Scientific).…”

“…During ripening, grape berries undergo a series of complex biochemical and physiological processes that enhance their quality for wine production but also their vulnerability to pathogen infection (Pezet et al, 2003;Deytieux-Belleau et al, 2009). Some ripening processes that may promote B. cinerea infections of grape berries are cell wall and cuticle modifications that lead to fruit softening and microfractures on the berry surface, modulation of the fruit's synthesis and perception of plant hormones, changes in the levels of organic acids and sugars, and the loss of preformed defenses (Miedes and Lorences, 2007;Cantu et al, 2008Cantu et al, , 2009Centeno et al, 2011;Blanco-Ulate et al, 2013b;Prusky et al, 2013). Moreover, B. cinerea infections can accelerate some of these ripening processes in unripe fruit (Cantu et al, 2009;Blanco-Ulate et al, 2013b;Agudelo-Romero et al, 2015).…”

Ripening of Tomato Fruit and Susceptibility to Botrytis cinerea

“…19.1 ), it had been thought that susceptibility is an inherent outcome of ripening (Prusky 1996 ;Klee and Giovannoni 2011 ). However, studies of the regulation of ripening and susceptibility have led to the conclusions that only selected ripening events and pathways are required to facilitate B. cinerea infections, and that B. cinerea modifi es its infection strategy as fruit ripen (Cantu et al 2008(Cantu et al , 2009Blanco-Ulate et al 2013.…”

“…It is also necessary to determine how B. cinerea impacts ripening by exploiting and diverting regulators and processes during fruit development. On unripe tomato fruit, B. cinerea accelerates selected aspects of ripening, thereby enhancing host susceptibility (Cristescu et al 2002 ;Cantu et al 2009 ;Blanco-Ulate et al 2013 ). How B. cinerea promotes susceptibility in fruit has not yet been determined, but toxins, plant hormone analogues, small RNAs and/or pathogen-and damage-associated molecular patterns (PAMPs and DAMPs, respectively) generated by B. cinerea during infections may be involved.…”

“…Infections of unripe fruit by B. cinerea could induce ethylene production under System 1 and consequently trigger plant defense responses, but could also prematurely activate System 2 and the consequent climacteric ripening or, in nonclimacteric fruit, initiate senescence or ripening pathways, which result in enhanced susceptibility that overthrows ethylene-induced defences (Marcos et al 2005 ;Swartzberg et al 2008 ;Cantu et al 2009 ;Blanco-Ulate et al 2013 ). When B. cinerea infects unripe tomato fruit, expression of two ACS genes from System 2, SlACS1a and SlACS2 , is precociously activated, suggesting that the pathogen activates ethylene synthesis by System 2 (Blanco-Ulate et al 2013 ).…”