TY - JOUR
T1 - Cooperation and coexpression
T2 - How coexpression networks shift in response to multiple mutualists
AU - Palakurty, Sathvik X.
AU - Stinchcombe, John R.
AU - Afkhami, Michelle E.
N1 - Funding Information:
National Science Foundation, Grant/Award Number: IOS-1401840; Natural Sciences and Engineering Research Council of Canada; University of Miami
Funding Information:
Many thanks to Wilson, Stinchcombe, Searcy and Afkhami laboratory groups as well as four anonymous reviewers and Editor Jacob Russell for feedback on this article. We also acknowledge NSF (IOS-1401840 to MEA), University of Miami, and NSERC (Discovery to JRS) for funding the research.
Publisher Copyright:
© 2018 John Wiley & Sons Ltd
PY - 2018/4
Y1 - 2018/4
N2 - A mechanistic understanding of community ecology requires tackling the nonadditive effects of multispecies interactions, a challenge that necessitates integration of ecological and molecular complexity—namely moving beyond pairwise ecological interaction studies and the “gene at a time” approach to mechanism. Here, we investigate the consequences of multispecies mutualisms for the structure and function of genomewide differential coexpression networks for the first time, using the tractable and ecologically important interaction between legume Medicago truncatula, rhizobia and mycorrhizal fungi. First, we found that genes whose expression is affected nonadditively by multiple mutualists are more highly connected in gene networks than expected by chance and had 94% greater network centrality than genes showing additive effects, suggesting that nonadditive genes may be key players in the widespread transcriptomic responses to multispecies symbioses. Second, multispecies mutualisms substantially changed coexpression network structure of 18 modules of host plant genes and 22 modules of the fungal symbionts’ genes, indicating that third-party mutualists can cause significant rewiring of plant and fungal molecular networks. Third, we found that 60% of the coexpressed gene sets that explained variation in plant performance had coexpression structures that were altered by interactive effects of rhizobia and fungi. Finally, an “across-symbiosis” approach identified sets of plant and mycorrhizal genes whose coexpression structure was unique to the multiple mutualist context and suggested coupled responses across the plant–mycorrhizal interaction to rhizobial mutualists. Taken together, these results show multispecies mutualisms have substantial effects on the molecular interactions in host plants, microbes and across symbiotic boundaries.
AB - A mechanistic understanding of community ecology requires tackling the nonadditive effects of multispecies interactions, a challenge that necessitates integration of ecological and molecular complexity—namely moving beyond pairwise ecological interaction studies and the “gene at a time” approach to mechanism. Here, we investigate the consequences of multispecies mutualisms for the structure and function of genomewide differential coexpression networks for the first time, using the tractable and ecologically important interaction between legume Medicago truncatula, rhizobia and mycorrhizal fungi. First, we found that genes whose expression is affected nonadditively by multiple mutualists are more highly connected in gene networks than expected by chance and had 94% greater network centrality than genes showing additive effects, suggesting that nonadditive genes may be key players in the widespread transcriptomic responses to multispecies symbioses. Second, multispecies mutualisms substantially changed coexpression network structure of 18 modules of host plant genes and 22 modules of the fungal symbionts’ genes, indicating that third-party mutualists can cause significant rewiring of plant and fungal molecular networks. Third, we found that 60% of the coexpressed gene sets that explained variation in plant performance had coexpression structures that were altered by interactive effects of rhizobia and fungi. Finally, an “across-symbiosis” approach identified sets of plant and mycorrhizal genes whose coexpression structure was unique to the multiple mutualist context and suggested coupled responses across the plant–mycorrhizal interaction to rhizobial mutualists. Taken together, these results show multispecies mutualisms have substantial effects on the molecular interactions in host plants, microbes and across symbiotic boundaries.
KW - RNA-Seq
KW - mycorrhizal fungi
KW - nonadditive
KW - rhizobia
KW - symbiosis
KW - transcriptome
KW - weighted gene coexpression network analysis
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U2 - 10.1111/mec.14550
DO - 10.1111/mec.14550
M3 - Article
C2 - 29533484
AN - SCOPUS:85045066251
VL - 27
SP - 1860
EP - 1873
JO - Molecular Ecology
JF - Molecular Ecology
SN - 0962-1083
IS - 8
ER -