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Insights on the Structural and Metabolic Resistance of Potato (Solanum tuberosum) Cultivars to Tuber Black Dot (Colletotrichum coccodes).

ABSTRACT: Black dot is a blemish disease of potato tubers caused by the phytopathogenic fungus Colletotrichum coccodes. Qualitative resistance (monogenic) that leads to the hypersensitive response has not been reported against black dot, but commercial potato cultivars show different susceptibility levels to the disease, indicating that quantitative resistance (polygenic) mechanisms against this pathogen exist. Cytological studies are essential to decipher pathogen colonization of the plant tissue, and untargeted metabolomics has been shown effective in highlighting resistance-related metabolites in quantitative resistance. In this study, we used five commercial potato cultivars with different susceptibility levels to black dot, and studied the structural and biochemical aspects that correlate with resistance to black dot using cytological and untargeted metabolomics methods. The cytological approach using semithin sections of potato tuber periderm revealed that C. coccodes colonizes the tuber periderm, but does not penetrate in cortical cells. Furthermore, skin thickness did not correlate with disease susceptibility, indicating that other factors influence quantitative resistance to black dot. Furthermore, suberin amounts did not correlate with black dot severity, and suberin composition was similar between the five potato cultivars studied. On the other hand, the untargeted metabolomics approach allowed highlighting biomarkers of infection, as well as constitutive and induced resistance-related metabolites. Hydroxycinnamic acids, hydroxycinnamic acid amides and steroidal saponins were found to be biomarkers of resistance under control conditions, while hydroxycoumarins were found to be specifically induced in the resistant cultivars. Notably, some of these biomarkers showed antifungal activity in vitro against C. coccodes. Altogether, our results show that quantitative resistance of potatoes to black dot involves structural and biochemical mechanisms, including the production of specialized metabolites with antifungal properties.

SUBMITTER: Massana-Codina J

PROVIDER: S-EPMC7468465 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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Insights on the Structural and Metabolic Resistance of Potato (Solanum tuberosum) Cultivars to Tuber Black Dot (Colletotrichum coccodes).

Massana-Codina Josep J Schnee Sylvain S Allard Pierre-Marie PM Rutz Adriano A Boccard Julien J Michellod Emilie E Cléroux Marilyn M Schürch Stéphanie S Gindro Katia K Wolfender Jean-Luc JL

Frontiers in plant science 20200820

Black dot is a blemish disease of potato tubers caused by the phytopathogenic fungus Colletotrichum coccodes. Qualitative resistance (monogenic) that leads to the hypersensitive response has not been reported against black dot, but commercial potato cultivars show different susceptibility levels to the disease, indicating that quantitative resistance (polygenic) mechanisms against this pathogen exist. Cytological studies are essential to decipher pathogen colonization of the plant tissue, ...[more]

PMID: 32973846

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Project description:BackgroundMost agronomic plant traits result from complex molecular networks involving multiple genes and from environmental factors. One such trait is the enzymatic discoloration of fruit and tuber tissues initiated by mechanical impact (bruising). Tuber susceptibility to bruising is a complex trait of the cultivated potato (Solanum tuberosum) that is crucial for crop quality. As phenotypic evaluation of bruising is cumbersome, the application of diagnostic molecular markers would empower the selection of low bruising potato varieties. The genetic factors and molecular networks underlying enzymatic tissue discoloration are sparsely known. Hitherto there is no association study dealing with tuber bruising and diagnostic markers for enzymatic discoloration are rare.ResultsThe natural genetic diversity for bruising susceptibility was evaluated in elite middle European potato germplasm in order to elucidate its molecular basis. Association genetics using a candidate gene approach identified allelic variants in genes that function in tuber bruising and enzymatic browning. Two hundred and five tetraploid potato varieties and breeding clones related by descent were evaluated for two years in six environments for tuber bruising susceptibility, specific gravity, yield, shape and plant maturity. Correlations were found between different traits. In total 362 polymorphic DNA fragments, derived from 33 candidate genes and 29 SSR loci, were scored in the population and tested for association with the traits using a mixed model approach, which takes into account population structure and kinship. Twenty one highly significant (p < 0.001) and robust marker-trait associations were identified.ConclusionsThe observed trait correlations and associated marker fragments provide new insight in the molecular basis of bruising susceptibility and its natural variation. The markers diagnostic for increased or decreased bruising susceptibility will facilitate the combination of superior alleles in breeding programs. In addition, this study presents novel candidates that might control enzymatic tissue discoloration and tuber bruising. Their validation and characterization will increase the knowledge about the underlying biological processes.

Project description:Maturation of potato (Solanum tuberosum L.) tuber native and wound periderm and development of resistance to periderm abrasion were investigated utilizing cytological and histochemical techniques. Both native and wound periderm consist of three different tissues: phellem, phellogen and phelloderm. It was previously determined that the phellogen walls of immature native periderm are thin and prone to fracture during harvest, leading to periderm abrasion (excoriation). Phellogen walls thicken and become less susceptible to fracture upon maturation of the periderm, leading to resistance to excoriation. We now demonstrate that phellogen cells of immature wound periderm also have thin radial walls and that wound periderm abrasion is due to fracture of these walls. Maturation of the wound periderm is also associated with an increase in the thickness of the phellogen radial walls. Histological analysis with ruthenium red and hydroxylamine-FeCI2, which stain unesterified and highly methyl-esterified pectins, respectively, indicates that the phellogen cell walls of native and wound periderm differ significantly regardless of the stage of maturity. Results obtained by staining with ruthenium red and hydroxylamine-FeCI2 imply that phellogen cell walls of immature native periderm contain methyl-esterified pectin, but are lacking in unesterified (acidic) pectins. Maturation of native periderm is accompanied by an apparent increase in unesterified pectins in the walls of phellogen cells, which may allow for the strengthening of phellogen cell walls via calcium pectate formation. Histological staining of the phellogen walls of wound periderm, on the other hand, implies that these walls are deficient in pectins. Moreover, maturation of wound periderm is not accompanied by an increase in unesterified pectins in these walls. Since peroxidase is known to catalyse the cross-linking of cell wall polymers, we stained native and wound periderm for the presence of peroxidase utilizing guaiacol as a substrate. Peroxidase staining was strong in the phellogen walls of both immature and mature native periderm and we could not detect any differences in staining between them. Peroxidase staining was weak in the phellogen walls of immature wound periderm and was not detectably different in mature wound periderm. Peroxidase data imply that there are distinct differences between native and wound periderm, though our data do not indicate that changes in peroxidase activity are involved in the development of resistance to periderm abrasion that occurs upon maturation of the periderm. However, we cannot rule out the involvement in this process of peroxidase isozymes that have low affinity for the substrates utilized here.

Dataset Information

Insights on the Structural and Metabolic Resistance of Potato (Solanum tuberosum) Cultivars to Tuber Black Dot (Colletotrichum coccodes).

Publications

Insights on the Structural and Metabolic Resistance of Potato (<i>Solanum tuberosum</i>) Cultivars to Tuber Black Dot (<i>Colletotrichum coccodes</i>).

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