Influence of water deficit on the molecular responses of Pinus contorta × Pinus banksiana mature trees to infection by the mountain pine beetle fungal associate, Grosmannia clavigera.

Adriana Arango-Velez,J E K Cooke,Jean Linsky,Inka Lusebrink,W El Kayal,L M G Gonzalez,B J Cooke,M J Meents,Barry J Cooke,Janice E K Cooke,Leonardo M Galindo González,Miranda J Meents,Walid El Kayal

doi:10.1093/treephys/tpt101

Abstract

Conifers exhibit a number of constitutive and induced mechanisms to defend against attack by pests and pathogens such as mountain pine beetle (Dendroctonus ponderosae Hopkins) and their fungal associates. Ecological studies have demonstrated that stressed trees are more susceptible to attack by mountain pine beetle than their healthy counterparts. In this study, we tested the hypothesis that water deficit affects constitutive and induced responses of mature lodgepole pine × jack pine hybrids (Pinus contorta Dougl. ex Loud. var. latifolia Engelm. ex S. Wats. × Pinus banksiana Lamb.) to inoculation with the mountain pine beetle fungal associate Grosmannia clavigera (Robinson-Jeffrey and Davidson) Zipfel, de Beer and Wingfield. The degree of stress induced by the imposed water-deficit treatment was sufficient to reduce photosynthesis. Grosmannia clavigera-induced lesions exhibited significantly reduced dimensions in water-deficit trees relative to well-watered trees at 5 weeks after inoculation. Treatment-associated cellular-level changes in secondary phloem were also observed. Quantitative RT-PCR was used to analyze transcript abundance profiles of 18 genes belonging to four families classically associated with biotic and abiotic stress responses: aquaporins (AQPs), dehydration-responsive element binding (DREB), terpene synthases (TPSs) and chitinases (CHIs). Transcript abundance profiles of a TIP2 AQP and a TINY-like DREB decreased significantly in fungus-inoculated trees, but not in response to water deficit. One TPS, Pcb(+)-3-carene synthase, and the Class II CHIs PcbCHI2.1 and PcbCHI2.2 showed increased expression under water-deficit conditions in the absence of fungal inoculation, while another TPS, Pcb(E)-β-farnesene synthase-like, and two CHIs, PcbCHI1.1 and PcbCHI4.1, showed attenuated expression under water-deficit conditions in the presence of fungal inoculation. The effects were observed both locally and systemically. These results demonstrate that both constitutive and induced carbon- and nitrogen-based defenses are affected by water deficit, suggesting potential consequences for mountain pine beetle dynamics, particularly in novel environments.

Highlights

The current outbreak of mountain pine beetle (MPB; Dendroctonus ponderasae Hopkins) has resulted in the loss of more than 28 million hectares of pine forest in western North America since 1999, including more than 19 million hectares in the western Canadian provinces of British Columbia and Alberta
We have examined the effect of water limitation on molecular defense responses of mature lodgepole × jack pine hybrid trees in central Alberta to the MPB fungal associate G. clavigera
Since no sequence resources were available for P. contorta × banksiana, we identified AQPand dehydration-responsive element binding (DREB)-like sequences for transcript abundance profiling by mining Sanger sequence data for pure P. contorta and P. banksiana

Summary

Introduction

The current outbreak of mountain pine beetle (MPB; Dendroctonus ponderasae Hopkins) has resulted in the loss of more than 28 million hectares of pine forest in western North America since 1999, including more than 19 million hectares in the western Canadian provinces of British Columbia and Alberta Wats.) × jack pine (Pinus banksiana Lamb.) hybrid zone in north-central Alberta, and more recently has undergone a host-shift expansion into pure jack pine, a boreal forest species with a range extending east to the Atlantic coast (Cullingham et al 2011). This unprecedented expansion of MPB into more northerly latitudes, into higher elevation forests and east into jack pine forests—all formerly considered marginal habitats for MPB—is postulated to have been facilitated at least in part by warmer than average temperatures during recent decades (Carroll et al 2004, Trenberth et al 2007)

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