Carica papaya Genes Regulated by Phytophthora palmivora: A Model System for Genomic Studies of Compatible Phytophthora-plant Interactions

Abstract

Plant pathogenic Phytophthora species are predicted to encode a large arsenal of 'effector' proteins that target and disrupt normal host cell function, but genes regulated by effectors are difficult to distinguish from those more generally regulated by microbe associated molecular patterns (MAMPs). To help make this distinction, expression studies of host-Phytophthora interactions can be compared to reveal patterns of gene regulation indicative of effector activity. The recently sequenced tropical fruit tree, Carica papaya, contains fewer genes than Arabidopsis and is highly susceptible to the broad-host-range pathogen P. palmivora, offering a new system for comparative genomics. In this study, genes isolated from the transcriptome of C. papaya seedling roots inoculated with P. palmivora, were evaluated for pathogen-regulation. Of these genes, a predicted peroxidase, ß-1,3-glucanase, ferulate 5-hydroxylase, and hypersensitive-induced response protein were pathogen upregulated, while a second peroxidase (Cp9) and aquaporin (Cp15), both with normally high root expression, were downregulated. Genes from other plants with similar expression responses to Phytophthora were identified from previously reported studies and evaluated for protein sequence similarity. Interestingly, as for papaya, Phytophthora also downregulates homologs of Cp9 and Cp15 in Glycine max and Solanum tuberosum, respectively. Because peroxidases associated with defense are generally upregulated during infection and the regulation of aquaporins have been cited in cases of both plant (Opperman et al. Science 263:221-223, 1994) and animal disease (Guttman et al. Cell Microbiol 9:131-141, 2007), Cp9 and Cp15 are potential cross-species effector targets. With whole-genome C. papaya microarrays forthcoming, this study highlights papaya as a resource for comparative genomic studies of Phytophthora-plant interaction.

Dual RNA-Sequencing of Eucalyptus nitens during Phytophthora cinnamomi Challenge Reveals Pathogen and Host Factors Influencing Compatibility

“…Peroxidases (PR-9) are potential cross-species Phytophthora effector targets, since a certain C. papaya peroxidase (EL784270) and its putative orthologs have been suppressed in different hosts upon inoculation with P. sojae, P. palmivora , and P. infestans (Moy et al, 2004 ; Restrepo et al, 2005 ; Porter et al, 2009 ). An E. grandis gene, Eucgr.E04056, is highly similar to the C. papaya ortholog, and is also strongly suppressed in the current interaction.…”

“…For example, P. infestans manipulates its host to suit its life-style by suppressing the hypersensitive response (HR) in potato during its biotrophic phase, then manipulating the induction of HR during the necrotrophic phase (Bos et al, 2010 ; Gilroy et al, 2011 ). This type of manipulation could be a trend in other Phytophthora interactions (Belhaj et al, 2009 ; Porter et al, 2009 ). Effectors excreted during this interaction are primarily crinklers (CRN), a family of proteins expressed in all plant pathogenic oomycetes, and RxLRs which are confined to only Phytophthora species (Stam et al, 2013b ; Chen et al, 2014 ).…”

Infection of Arabidopsis thaliana by Phytophthora parasitica and identification of variation in host specificity

“…Among the 19 genes significantly up‐regulated in A. thaliana in response to P. parasitica infection, signature sequences characteristic of biotic stresses were notable. For example, a homologue of TC1736, which encodes a putative peroxidase, was identified to be up‐regulated in papaya challenged with P. palmivora (Porter et al ., 2009). The homologues of TC2158, TC2086 and TC1736 were reported to be up‐regulated by twofold or more in soybean infected with P. sojae (Moy et al ., 2004).…”

Dual RNA-Sequencing Analysis of Resistant (Pinus pinea) and Susceptible (Pinus radiata) Hosts during Fusarium circinatum Challenge

“…Other PR proteins such as peroxidases (PR9) were up- and down-regulated in P. pinea , similar to the interaction of P. pinaster - F. circinatum at 10 dpi [ 42 ] and Eucalyptus nitens - Phytophthora cinnamomi at 5 dpi [ 36 ]. This could point out pine PR9 as effector target of F. circinatum , which has been found in several Phytophthora species infecting Carica papaya [ 86 , 87 , 88 ]. It has been suggested that activation of PR genes, notably plant chitinases, is produced mainly in susceptible Pinus spp.…”