Abstract
BackgroundRiverine ecosystems, highly sensitive to climate change and human activities, are characterized by rapid environmental change to fluctuating water levels and siltation, causing stress on their biological components. We have little understanding of mechanisms by which riverine plant species have developed adaptive strategies to cope with stress in dynamic environments while maintaining growth and development.ResultsWe report that poplar (Populus spp.) has evolved a systems level "stress proteome" in the leaf-stem-root apoplast continuum to counter biotic and abiotic factors. To obtain apoplast proteins from P. deltoides, we developed pressure-chamber and water-displacement methods for leaves and stems, respectively. Analyses of 303 proteins and corresponding transcripts coupled with controlled experiments and bioinformatics demonstrate that poplar depends on constitutive and inducible factors to deal with water, pathogen, and oxidative stress. However, each apoplast possessed a unique set of proteins, indicating that response to stress is partly compartmentalized. Apoplast proteins that are involved in glycolysis, fermentation, and catabolism of sucrose and starch appear to enable poplar to grow normally under water stress. Pathogenesis-related proteins mediating water and pathogen stress in apoplast were particularly abundant and effective in suppressing growth of the most prevalent poplar pathogen Melampsora. Unexpectedly, we found diverse peroxidases that appear to be involved in stress-induced cell wall modification in apoplast, particularly during the growing season. Poplar developed a robust antioxidative system to buffer oxidation in stem apoplast.ConclusionThese findings suggest that multistress response in the apoplast constitutes an important adaptive trait for poplar to inhabit dynamic environments and is also a potential mechanism in other riverine plant species.
Highlights
Riverine ecosystems, highly sensitive to climate change and human activities, are characterized by rapid environmental change to fluctuating water levels and siltation, causing stress on their biological components
Extracting protein-containing poplar apoplast fluid Obtaining a population of representative apoplast proteins from various tissues in poplar without symplastic contamination is technically challenging
The large subunit of ribulose-bisphosphate carboxylase, which is symplast specific [25], was abundant in whole leaf tissues, whereas it was undetectable in the apoplast
Summary
Highly sensitive to climate change and human activities, are characterized by rapid environmental change to fluctuating water levels and siltation, causing stress on their biological components. Riverine ecosystems, characterized with rapid and dramatic environmental changes caused by fluctuating water levels and siltation, harbor a number of plants, including many species of the fast growing, ecological pioneers such as perennial poplar (Populus spp.; [1,2,3,4,5]). These species have a dramatic influence on ecosystem cycles. The apoplast represents a highly dynamic compartment serving as a continuum from roots through the stem to leaves and is potentially important as a bridge that perceives and transduces signals from the environment to the symplast
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