Apoplast proteome reveals that extracellular matrix contributes to multistress response in poplar Public

Olga Pechanova, Chuan-Yu Hsu, Joshua P. Adams, Tibor Pechan, Lindsay Vandervelde, Jenny Drnevich, Sara Jawdy, Ardeshir Adeli, Jeffrey C. Suttle, Amanda M. Lawrence, Timothy J. Tschaplinski, Armand Seguin and Cetin Yuceer 2010 November 29 BMC Genomics 2010, 11:674 doi:10.1186/1471-2164-11-674
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Background 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. 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. Results We 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. Conclusion These 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.


Our study shows that poplar has developed a diverse apoplast proteome in the leaf-stem-root continuum. Such a complex proteome appears to play a major role in mediating water, pathogen, and oxidative stress, suggesting that a systems level mechanism has evolved in poplar apoplast allowing encounters of multiple stresses while maintaining growth and development over many years. We anticipate our work to be a starting point for developing a systems level understanding of how the extracellular matrix mediates multistress responses in plant species of riverine ecosystems under fluctuating environmental conditions.

(A) Average monthly high and low temperatures, precipitation, and day-length from 2003 to 2007. Orange-color shows the sampling time of tissues for apoplast proteome, whereas the shaded background indicates the sampling of leaf tissues for transcript analysis using microarrays. Developmental stages of leaves and shoots are shown on the right during sampling. Bar = 2 mm (September-March) and = 1 cm (April-August). (B) High/low temperatures and precipitation during sampling for apoplast proteome analysis (April-July, 2007). Arrows indicate flooding times. The red bar shows normal Melampsora infestation. (C-E) Quantitative distribution of leaf and stem apoplast proteins. 84 proteins (38+46) were detected with 2-D PAGE, whereas 106 proteins (60+46) were detected with 2-D LC. Both 2-D PAGE and 2-D LC detected 46 proteins. (F) Quantitative distribution of leaf, stem, and root apoplast proteins. 2-D PAGE-based poplar root apoplast proteome was from Dafoe and Constabel [22]. Functional classification of leaf (G) and stem (H) apoplast proteins.

Poplar leaf, stem, and root apoplast protein IDs are shown in colored numbers. The metabolic pathways were modified from Srivastava [138], Kreuzwieser et al [38], Magneschi and Perata [139], and Narsai et al [140].

(A) Year-round transcript levels of P. deltoides leaf apoplast proteins using poplar microarrays, and hierarchical clustering of the transcripts corresponding to 139 proteins. Transcript abundance over time is represented as the log2 fold-change of each time point to the baseline time point (September). Vertical bars with a color represent a module. Functional classification of each module is shown on the right with the number (n) of genes. (B) Heat map showing response of genes corresponding to apoplast proteins at the transcript level to water stress in P. deltoides that was subjected to moderate (-0.49 MPa) to severe (-1.26 MPa) cyclical water stress. Expression less than 1.0 is down-regulated compared to control, whereas expression greater than 1.0 is up-regulated. (C-E) Transcript response of genes corresponding to apoplast proteins in leaves when poplar NM6 (P. nigra X P. maximowiczii) was challenged with the isolates of M. medusae f. sp. deltoidae (Mmd) and M. laricipopulina (Mlp). Control (ctrl) tissues were also analyzed. Error bars show standard deviation about the mean.


Pechanova O, Hsu CY, Adams JP, Pechan T, Vandervelde L, Drnevich J, Jawdy S, Adeli A, Suttle JC, Lawrence AM, Tschaplinski TJ, S├ęguin A, Yuceer C. Apoplast proteome reveals that extracellular matrix contributes to multistress response in poplar. BMC Genomics. 2010 Nov 29;11:674. doi: 10.1186/1471-2164-11-674. PubMed PMID: 21114852; PubMed Central PMCID: PMC3091788.

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