Lineage-specific expression divergence in grasses is associated with Male reproduction, host-pathogen defense, and domestication

Raquel Assis

Research output: Contribution to journalArticle

Abstract

Poaceae (grasses) is an agriculturally important and widely distributed family of plants with extraordinary phenotypic diversity, much of which was generated under recent lineage-specific evolution. Yet, little is known about the genes and functional modules involved in the lineage-specific divergence of grasses. Here, I address this question on a genome-wide scale by applying a novel branch-based statistic of lineage-specific expression divergence, LED, to RNA-seq data from nine tissues of the wild grass Brachypodium distachyon and its domesticated relatives Oryza sativa japonica (rice) and Sorghum bicolor (sorghum). I find that LED is generally smallest in B. distachyon and largest in O. sativa japonica, which underwent domestication earlier than S. bicolor, supporting the hypothesis that domestication may increase the rate of lineage-specific expression divergence in grasses. Moreover, in all three species, LED is positively correlated with protein-coding sequence divergence and tissue specificity, and negatively correlated with network connectivity. Further analysis reveals that genes with large LED are often primarily expressed in anther, implicating lineage-specific expression divergence in the evolution of male reproductive phenotypes. Gene ontology enrichment analysis also identifies an overrepresentation of terms related to male reproduction in the two domesticated grasses, as well as to those involved in host-pathogen defense in all three species. Last, examinations of genes with the largest LED reveal that their lineage-specific expression divergence may have contributed to antimicrobial functions in B. distachyon, to enhanced adaptation and yield during domestication in O. sativa japonica, and to defense against a widespread and devastating fungal pathogen in S. bicolor. Together, these findings suggest that lineage-specific expression divergence in grasses may increase under domestication and preferentially target rapidly evolving genes involved in male reproduction, host-pathogen defense, and the origin of domesticated phenotypes.

Original languageEnglish (US)
Pages (from-to)207-219
Number of pages13
JournalGenome biology and evolution
Volume11
Issue number1
DOIs
StatePublished - Jan 1 2019

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domestication
Poaceae
Reproduction
pathogen
divergence
grass
Brachypodium distachyon
Brachypodium
Sorghum
grasses
pathogens
Sorghum bicolor
Oryza sativa
gene
genes
sorghum
phenotype
Genes
Phenotype
Organ Specificity

All Science Journal Classification (ASJC) codes

  • Ecology, Evolution, Behavior and Systematics
  • Genetics

Cite this

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title = "Lineage-specific expression divergence in grasses is associated with Male reproduction, host-pathogen defense, and domestication",
abstract = "Poaceae (grasses) is an agriculturally important and widely distributed family of plants with extraordinary phenotypic diversity, much of which was generated under recent lineage-specific evolution. Yet, little is known about the genes and functional modules involved in the lineage-specific divergence of grasses. Here, I address this question on a genome-wide scale by applying a novel branch-based statistic of lineage-specific expression divergence, LED, to RNA-seq data from nine tissues of the wild grass Brachypodium distachyon and its domesticated relatives Oryza sativa japonica (rice) and Sorghum bicolor (sorghum). I find that LED is generally smallest in B. distachyon and largest in O. sativa japonica, which underwent domestication earlier than S. bicolor, supporting the hypothesis that domestication may increase the rate of lineage-specific expression divergence in grasses. Moreover, in all three species, LED is positively correlated with protein-coding sequence divergence and tissue specificity, and negatively correlated with network connectivity. Further analysis reveals that genes with large LED are often primarily expressed in anther, implicating lineage-specific expression divergence in the evolution of male reproductive phenotypes. Gene ontology enrichment analysis also identifies an overrepresentation of terms related to male reproduction in the two domesticated grasses, as well as to those involved in host-pathogen defense in all three species. Last, examinations of genes with the largest LED reveal that their lineage-specific expression divergence may have contributed to antimicrobial functions in B. distachyon, to enhanced adaptation and yield during domestication in O. sativa japonica, and to defense against a widespread and devastating fungal pathogen in S. bicolor. Together, these findings suggest that lineage-specific expression divergence in grasses may increase under domestication and preferentially target rapidly evolving genes involved in male reproduction, host-pathogen defense, and the origin of domesticated phenotypes.",
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Lineage-specific expression divergence in grasses is associated with Male reproduction, host-pathogen defense, and domestication. / Assis, Raquel.

In: Genome biology and evolution, Vol. 11, No. 1, 01.01.2019, p. 207-219.

Research output: Contribution to journalArticle

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