Abstract

BackgroundAge-related resistance (ARR) is a developmentally regulated phenomenon conferring resistance to pathogens or pests. Although ARR has been observed in several host-pathogen systems, the underlying mechanisms are largely uncharacterized. In cucumber, rapidly growing fruit are highly susceptible to Phytophthora capsici but become resistant as they complete exponential growth. We previously demonstrated that ARR is associated with the fruit peel and identified gene expression and metabolomic changes potentially functioning as preformed defenses.ResultsHere, we compare the response to infection in fruit at resistant and susceptible ages using microscopy, quantitative bioassays, and weighted gene co-expression analyses. We observed strong transcriptional changes unique to resistant aged fruit 2–4 h post inoculation (hpi). Microscopy and bioassays confirmed this early response, with evidence of pathogen death and infection failure as early as 4 hpi and cessation of pathogen growth by 8–10 hpi. Expression analyses identified candidate genes involved in conferring the rapid response including those encoding transcription factors, hormone signaling pathways, and defenses such as reactive oxygen species metabolism and phenylpropanoid biosynthesis.ConclusionThe early pathogen death and rapid defense response in resistant-aged fruit provide insight into potential mechanisms for ARR, implicating both pre-formed biochemical defenses and developmentally regulated capacity for pathogen recognition as key factors shaping age-related resistance.

Highlights

  • Age-related resistance (ARR) is a developmentally regulated phenomenon conferring resistance to pathogens or pests

  • The cultivar ‘Poinsett 76’ displays age-related resistance to P. capsici Our previous ARR studies [6, 13,14,15] examined ‘Vlaspik’, an F1 hybrid commonly grown for processing cucumber production in the midwestern USA

  • The unwounded fruit surface was inoculated with droplets of P. capsici zoospore suspension and evaluated over a period of ten days using a 9-point disease score rating (Supplementary Table 1)

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Summary

Introduction

Age-related resistance (ARR) is a developmentally regulated phenomenon conferring resistance to pathogens or pests. Developmental, or age-related resistance (ARR), wherein plants or plant organs transition from susceptibility to resistance as a result of developmental changes [1,2,3], has been described in several different plant-pathogen systems and in crops such as pepper, grape, rice, wheat, and several. In Arabidopsis, transcriptional control of the canonical immune receptor FLS2 was shown to regulate ontogenic resistance to Pseudomonas syringae [12] In these examples, a newly acquired ability to perceive the pathogen allows for an induced resistance response at the resistant age. One model system for organ specific ARR is cucumber fruit rot by the oomycete Phytophthora capsici [13,14,15] This soilborne hemibiotroph is a pathogen of many agriculturally important crops including numerous solanaceous and cucurbit species [16]. Two major transcriptomic responses were identified: 1) at initial infection (8 hpi) at which host primary metabolism was downregulated and specialized metabolism was upregulated, and 2) at the transition to necrotrophy (48 hpi) when large scale transcriptional reprograming occurs in the host [19]

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