Proteometabolomic Study of Compatible Interaction in Tomato Fruit Challenged with Sclerotinia rolfsii Illustrates Novel Protein Network during Disease Progression

Abstract

Fruit is an assimilator of metabolites, nutrients, and signaling molecules, thus considered as potential target for pathogen attack. In response to patho-stress, such as fungal invasion, plants reorganize their proteome, and reconfigure their physiology in the infected organ. This remodeling is coordinated by a poorly understood signal transduction network, hormonal cascades, and metabolite reallocation. The aim of the study was to explore organ-based proteomic alterations in the susceptibility of heterotrophic fruit to necrotrophic fungal attack. We conducted time-series protein profiling of Sclerotinia rolfsii invaded tomato (Solanum lycopersicum) fruit. The differential display of proteome revealed 216 patho-stress responsive proteins (PSRPs) that change their abundance by more than 2.5-fold. Mass spectrometric analyses led to the identification of 56 PSRPs presumably involved in disease progression; regulating diverse functions viz. metabolism, signaling, redox homeostasis, transport, stress-response, protein folding, modification and degradation, development. Metabolome study indicated differential regulation of organic acid, amino acids, and carbohydrates paralleling with the proteomics analysis. Further, we interrogated the proteome data using network analysis that identified two significant functional protein hubs centered around malate dehydrogenase, T-complex protein 1 subunit gamma, and ATP synthase beta. This study reports, for the first-time, kinetically controlled patho-stress responsive protein network during post-harvest storage in a sink tissue, particularly fruit and constitute the basis toward understanding the onset and context of disease signaling and metabolic pathway alterations. The network representation may facilitate the prioritization of candidate proteins for quality improvement in storage organ.

Proteomics of Reproductive Development, Fruit Ripening, and Stress Responses in Tomato

“…Organic acids such as oxalic acids have been reported to degrade cell walls through the chelation of Ca 2+ ions and the downregulation of Ca 2+ -mediated signaling pathways that regulate fruit ripening. In transgenic tomatoes where the synthesis of oxalic acid was repressed, an enhanced organoleptic property of the fruit and the increased resistance of the plant to necrotrophic fungus were observed . Some proteins that have been identified by further studies in oxalate-downregulated lines include chaperonins, Hsps, peptide methionine sulfoxide reductase, 26S protease regulatory subunit 7, peroxiredoxins, MDHAR, and ubiquitin interactors such as 14–3–3 ligase .…”

“…Enzymes that are essential in carbon, amino acid, and fatty acid metabolism play a concerted role in organizing the physiology of the host during infection. Some key upregulated proteins during S. rolfsii infection include aldo-keto reductase, which is known to increase mannitol content, β-fructofuranosidase, enolase, methionine sulfoxide reductase, acetylornithine deacetylase, and some chaperones such asDnaK …”

“…In transgenic tomatoes where the synthesis of oxalic acid was repressed, an enhanced organoleptic property of the fruit and the increased resistance of the plant to necrotrophic fungus were observed. 94 Some proteins that have been identified by further studies in oxalatedownregulated lines include chaperonins, Hsps, peptide methionine sulfoxide reductase, 26S protease regulatory subunit 7, peroxiredoxins, MDHAR, and ubiquitin interactors such as 14−3−3 ligase. 95 Other proteins, viz.…”

“…Some key upregulated proteins during S. rolfsii infection include aldo-keto reductase, which is known to increase mannitol content, β-fructofuranosidase, enolase, methionine sulfoxide reductase, acetylornithine deacetylase, and some chaperones such asDnaK. 172 Plant hormone jasmonic acid (JA) promotes the hypersensitive response of plants by inducing PCD via coronatine insensitive 1 (COI1)-dependent signaling. The proteome of the leaves of tomato that were infected with Alternaria alternata f.sp.…”

Trait discovery and editing in tomato

“…Examples of these are rootstock grafting (Ntatsi et al ., ), effect of root mycorhization on fruit quality (Zouari et al ., ), meristem maturation and inflorescence architecture (Park et al ., ; Soyk et al ., ), leaf morphology and thickness (Koenig et al ., ; Coneva et al ., ), glandular trichome metabolism (Balcke et al ., ), seed composition (Toubiana et al ., ), fruit set and parthenocarpy (Wang et al ., ; Ruiu et al ., ), and fruit development, ripening, and composition (Carrari et al ., ; Faurobert et al ., ; Mintz‐Oron et al ., ; Mounet et al ., ; Matas et al ., ; Osorio et al ., ; Itkin et al ., ; Pan et al ., ; Pattison et al ., ; Fernandez‐Moreno et al ., ; Szymanski et al ., ; Li et al ., ; Shinozaki et al ., ; Stevens et al ., ). While fruit studies outnumber all others, considerable efforts have also been devoted to the study of abiotic stress, including heat (Keller and Simm, ), cold (Cruz‐Mendívil et al ., ; Barrero‐Gil et al ., ; Ntatsi et al ., ), water limitation (Albert et al ., ), salinity stress (Zhang et al ., ) and nutrient deficiency (Zamboni et al ., ), and of plant reaction to biotic stress, causes of which include viruses (Ramesh et al ., ), bacteria (French et al ., ), fungi (Blanco‐Ulate et al ., ; Ghosh et al ., ), and nematodes (Święcicka et al ., ).…”