Abstract
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.
| Original language | English (US) |
|---|---|
| Pages (from-to) | 1860-1873 |
| Number of pages | 14 |
| Journal | Molecular Ecology |
| Volume | 27 |
| Issue number | 8 |
| DOIs | |
| State | Published - Apr 1 2018 |
Fingerprint
Keywords
- mycorrhizal fungi
- nonadditive
- rhizobia
- RNA-Seq
- symbiosis
- transcriptome
- weighted gene coexpression network analysis
ASJC Scopus subject areas
- Ecology, Evolution, Behavior and Systematics
- Genetics
Cite this
Cooperation and coexpression : How coexpression networks shift in response to multiple mutualists. / Palakurty, Sathvik X.; Stinchcombe, John R.; Afkhami, Michelle.
In: Molecular Ecology, Vol. 27, No. 8, 01.04.2018, p. 1860-1873.Research output: Contribution to journal › Article
}
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
PY - 2018/4/1
Y1 - 2018/4/1
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 - mycorrhizal fungi
KW - nonadditive
KW - rhizobia
KW - RNA-Seq
KW - symbiosis
KW - transcriptome
KW - weighted gene coexpression network analysis
UR - http://www.scopus.com/inward/record.url?scp=85045066251&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=85045066251&partnerID=8YFLogxK
U2 - 10.1111/mec.14550
DO - 10.1111/mec.14550
M3 - Article
VL - 27
SP - 1860
EP - 1873
JO - Molecular Ecology
JF - Molecular Ecology
SN - 0962-1083
IS - 8
ER -