The Transcriptional Response of Hybrid Poplar (Populus trichocarpa x P. deltoids) to Infection by Melampsora medusae Leaf Rust Involves Induction of Flavonoid Pathway Genes Leading to the Accumulation of Proanthocyanidins

Abstract

The transcriptional response of hybrid poplar (Populus trichocarpa x P. deltoides) to poplar leaf rust (Melampsora medusae) infection was studied using the Populus 15.5K cDNA microarray. Pronounced changes in the transcriptome were observed, with approximately 20% of genes on the array showing either induction or repression of transcription within the 9-day infection timecourse. A small number of pathogen-defense genes encoding PR-1, chitinases, and other pathogenesis-related proteins were consistently upregulated throughout the experimental period, but most genes were affected only at individual timepoints. The largest number of changes in gene expression was observed late in the infection at 6 to 9 days postinoculation (dpi). At these timepoints, genes encoding enzymes required for proanthocyanidin (condensed tannin) synthesis were upregulated dramatically. Phytochemical analysis confirmed that, late in the infection, proanthocyanidin levels increased in infected leaves. Strongly M. medusae-repressed genes at 9 dpi included previously characterized wound- and herbivore-induced defense genes, which suggests antagonism between the tree responses to insect feeding and M. medusae infection. In this highly compatible plant-pathogen interaction, we postulate that the biotrophic pathogen evades detection and suppresses early host responses.

The MYB182 Protein Down-Regulates Proanthocyanidin and Anthocyanin Biosynthesis in Poplar by Repressing Both Structural and Regulatory Flavonoid Genes

“…For example, two UGTs are repressed by MYB182, including UGT78M1, an enzyme that we had found to be induced in Melampsora medusae-infected poplar leaves (Miranda et al, 2007). However, the recombinant UGT78M1 protein was not active with any anthocyanin, flavonol, or flavan-3-ol substrate that we tested, so its biochemical function remains undefined (Veljanovski and Constabel, 2013).…”

Mechanisms of plant defense against insect herbivores

“…Although induced responses have some metabolic costs, 13 they are very important when aimed at alleviating the stress of immediate concern, as most of these chemicals are produced in response to herbivore attack. 14,15 Induced defenses make the plants phenotypically plastic, and thereby, decrease the chances of the attacking insects to adapt to the induced chemicals. 1,12 Changes in defensive constituents of a plant on account of insect attack develop unpredictability in the plant environment for insect herbivores, which in turn, affects the fitness and behavior of the herbivores.…”

“…1,12 Changes in defensive constituents of a plant on account of insect attack develop unpredictability in the plant environment for insect herbivores, which in turn, affects the fitness and behavior of the herbivores. 5,6,14 If induced response occurs very early, it is of great benefit to the plant, and reduces the subsequent herbivore and pathogen attack, besides improving overall fitness of the plant. 12 Plants with high variability in defensive chemicals exhibit a better defense compared with those with moderate variability.…”

“…45 Genes responsible for the production of tannins in response to wounding have been identified and are activated by the expression of a condensed tannins regulatory gene, PtMYB134, which is itself induced by damage. 53 Furthermore, induction of tannin is also stimulated by light stress, 14,53 and exposure to UV light in hybrid poplar. 53 However, some polyphagous insect species have the ability to tolerate gallotannins, e.g., Shistocerca gregaria (Forsk.)…”

Regulation of stilbene biosynthesis in plants

“…Flavonoid production is known to be induced in response to various environmental stresses and nutritional factors, e.g., microbial and virus infections, high-light stress, UV irradiation, unfavorable temperatures, drought, or increased sucrose concentrations (Miranda et al 2007;Gutha et al 2010;Ferri et al 2011;Zhang et al 2012;Nakabayashi et al 2014;Degu et al 2016). These factors modulate different regulatory proteins that control flavonoid biosynthesis by regulating transcription of the genes encoding flavonoid biosynthesis enzymes or transcription factors.…”