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Title: An ABC Transporter Mutation Alters Root Exudation of Phytochemicals that Provoke an Overhaul of Natural Soil Microbiota.

Author
item QUINTANA, NAIRA - Colorad0 State University
item BADRI, DAYAKAR - Colorad0 State University
item KASSIS, EKIE - Colorad0 State University
item KIM, HYE - Leiden University Medical Center
item CHOI, YOUNG - Leiden University Medical Center
item VERPOORTE, ROBERT - Leiden University Medical Center
item MARTINOIA, ENRICO - University Of Zurich
item Manter, Daniel
item VIVANCO, JORGE - Colorad0 State University

Submitted to: Journal of Plant Physiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/19/2009
Publication Date: 10/23/2009
Citation: Quintana, N., Badri, D., Kassis, E., Kim, H., Choi, Y., Verpoorte, R., Martinoia, E., Manter, D.K., Vivanco, J. 2009. An ABC Transporter Mutation Alters Root Exudation of Phytochemicals that Provoke an Overhaul of Natural Soil Microbiota. Journal of Plant Physiology. 151:2006-2017.

Interpretive Summary: Root exudates influence the surrounding soil microbial community, and recent evidence demonstrates the involvement of ATP-binding cassette (ABC) transporters in root secretion of phytochemicals. In this study, we examined effects of seven Arabidopsis (Arabidopsis thaliana) ABC transporter mutants on the microbial community in native soils. After two generations, only the Arabidopsis abcg30 (Atpdr2) mutant had significantly altered both the fungal and bacterial communities compared with the wild type using automated ribosomal intergenic spacer analysis. Similarly, root exudate profiles differed between the mutants; however, the largest variance from the wild type (Columbia-0) was observed in abcg30, which showed increased phenolics and decreased sugars. In support of this biochemical observation, whole-genome expression analyses of abcg30 roots revealed that some genes involved in biosynthesis and transport of secondary metabolites were up-regulated, while some sugar transporters were down-regulated compared with genome expression in wild-type roots. Microbial taxa associated with Columbia-0 and abcg30 cultured soils determined by pyrosequencing revealed that exudates from abcg30 cultivated a microbial community with a relatively greater abundance of potentially beneficial bacteria (i.e. plant-growth-promoting rhizobacteria and nitrogen fixers) and were specifically enriched in bacteria involved in heavy metal remediation. In summary, we report how a single gene mutation from a functional plant mutant influences the surrounding community of soil organisms, showing that genes are not only important for intrinsic plant physiology but also for the interactions with the surrounding community of organisms as well.

Technical Abstract: It has been shown that Arabidopsis root exudates can support the fungal community in native soils but not in non-native soils and recent evidence demonstrates the involvement of ABC transporters in the root secretion of phytochemicals. In this paper we examined differences in the root exudate profile of eight Arabidopsis ABC transporter mutants (ath6, mrp2, pdr2, pdr6, pdr7, pgp1, pgp4 and tap2), and the ability of these mutants to regulate the microbial community in a native Arabidopsis soil. Although the root exudates differed in many of the mutant lines, the largest difference from the wild type (Col-0) was observed with the pdr2 mutant. A 2-D NMR analysis of the root exudate profiles of pdr2 and Col-0 showed that they differed by nearly 20% - largely due to an increase in phenolic compounds, and a decline in sugars. Interestingly, only pdr2 caused a significant re-arrangement of both the fungal and bacterial communities compared with the wild type, based on both automated ribosomal intergenic spacer analysis (ARISA) and pyrosequencing. Changes of particular interest in the pdr2 community include an increase in several potential plant growth promoting bacteria (Brevundimonas sp. and Pseudomonas sp); increases in bacteria related to heavy metal remediation (Sphingomonas sp. and Methylobacterium sp.); and declines in several potential fungal pathogens (Agrobacterium sp. and Streptomyces sp.). To the best of our knowledge, this is the first report of a single plant gene mutation influencing the surrounding soil microbial community and suggests that ABC transporter mutants are key models to further elucidate the chemical linkage between plants and soil microbes.