Successive evolutionary steps drove Pooideae grasses from tropical to temperate regions

Zhong, Jinshun; Robbett, Meghan; Poire, Alfonso; Preston, Jill C.

doi:10.1111/nph.14868

Cited by 32 publications

(35 citation statements)

References 80 publications

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“…S2B). These results indicate that the evolution of cold acclimation evolved at least partly independently in separate lineages and are in line with recent work on transcriptional responses to vernalization in Pooideae (McKeown et al, 2016;Zhong et al, 2018).…”

Section: Cold Acclimation Evolved Independently In Separate Lineagessupporting

confidence: 91%

Evolution of Cold Acclimation and Its Role in Niche Transition in the Temperate Grass Subfamily Pooideae

et al. 2019

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The grass subfamily Pooideae dominates the grass floras in cold temperate regions and has evolved complex physiological adaptations to cope with extreme environmental conditions like frost, winter, and seasonality. One such adaptation is cold acclimation, wherein plants increase their frost tolerance in response to gradually falling temperatures and shorter days in the autumn. However, understanding how complex traits like cold acclimation evolve remains a major challenge in evolutionary biology. Here, we investigated the evolution of cold acclimation in Pooideae and found that a phylogenetically diverse set of Pooideae species displayed cold acclimation capacity. However, comparing differential gene expression after cold treatment in transcriptomes of five phylogenetically diverse species revealed widespread species-specific responses of genes with conserved sequences. Furthermore, we studied the correlation between gene family size and number of cold-responsive genes as well as between selection pressure on coding sequences of genes and their cold responsiveness. We saw evidence of protein-coding and regulatory sequence evolution as well as the origin of novel genes and functions contributing toward evolution of a cold response in Pooideae. Our results reflect that selection pressure resulting from global cooling must have acted on already diverged lineages. Nevertheless, conservation of cold-induced gene expression of certain genes indicates that the Pooideae ancestor may have possessed some molecular machinery to mitigate cold stress. Evolution of adaptations to seasonally cold climates is regarded as particularly difficult. How Pooideae evolved to transition from tropical to temperate biomes sheds light on how complex traits evolve in the light of climate changes.

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Section: Cold Acclimation Evolved Independently In Separate Lineagessupporting

confidence: 91%

Evolution of Cold Acclimation and Its Role in Niche Transition in the Temperate Grass Subfamily Pooideae

et al. 2019

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“…This hypothesis is supported by two recent studies. In a study of three Pooideae species, Zhong, Robbett, Poire, & Preston (2018) identified several gene clusters exhibiting conserved cold response, many of which had previously been characterized as ancient stress response genes. Another study found 16 cold-responsive genes that exhibited conserved expression in five distantly related Pooideae species (Schubert, Grønvold, Sandve, Hvidsten, & Fjellheim, 2019).…”

Section: Frost Tolerance and Ancestral Nichementioning

confidence: 99%

The grass subfamily Pooideae: Cretaceous–Palaeocene origin and climate‐driven Cenozoic diversification

Schubert

Marcussen

Meseguer

et al. 2019

Global Ecol Biogeogr

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Aim Frost is among the most dramatic stresses a plant can experience, and complex physiological adaptations are needed to endure long periods of sub‐zero temperatures. Owing to the need to evolve these complex adaptations, transitioning from tropical to temperate climates is regarded as difficult. Here, we study the transition from tropical to temperate climates in the grass subfamily Pooideae, which dominates cool temperate, continental and Arctic regions. We produce a dated phylogeny and investigate the role of climate cooling in diversification. Location Global, temperate regions. Time period Cretaceous–Cenozoic. Major taxa Pooideae. Methods Using newly available fossils and methods, we dated a comprehensive Pooideae phylogeny and tested for the impact of palaeoclimates on diversification rates. Using ancestral state reconstruction, we investigated whether Pooideae ancestors experienced frost and winter. To locate the ancestral distribution area of Pooideae, we performed biogeographical analyses. Results We estimated a Late Cretaceous/early Palaeocene origin of the Pooideae (61–77 Ma), with all major clades already having diversified at the Eocene–Oligocene climate cooling (34 Ma). Climate cooling was a probable driving force of Pooideae diversification. Pooideae probably evolved in a temperate niche experiencing frost, but not long winters. Main conclusion Pooideae probably originated in a temperate niche and experienced cold temperatures and frost long before expansion of temperate biomes after the Eocene–Oligocene transition. This suggests that the Pooideae ancestor had adaptations to temperate climate and that certain responses to low‐temperature stress are shared in extant Pooideae grasses. Throughout the Cenozoic, falling temperatures and expansion of temperate biomes were associated with an increase in diversification. However, complex mechanisms for enduring strongly seasonal climate with long, cold winters most probably evolved independently in daughter lineages. Our findings provide insight into how adaptations to historical changes in chill and frost exposure influence the distribution of plant diversity today.

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“…This hypothesis is supported by two recent studies. In a study of three Pooideae species, Zhong, Robbett, Poire, & Preston (2017) identified several gene clusters exhibiting conserved cold response, many of which had previously been characterized as ancient stress response genes. Another study found sixteen cold responsive genes that exhibited conserved expression in five distantly related Pooideae species (Schubert et al, unpublished).…”

Section: Did the Pooideae Ancestor Live In Cold Microhabitats?mentioning

confidence: 99%

The grass subfamily Pooideae: late Cretaceous origin and climate-driven Cenozoic diversification

Schubert

Marcussen

Meseguer

et al. 2018

Preprint

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 Aim: Frost is among the most dramatic stresses a plant can experience and complex physiological adaptations are needed to endure long periods of sub-zero temperatures. Due to the need for evolving these complex adaptations, transitioning from tropical to temperate climates is regarded difficult and only half of the world's seed plant families have temperate representatives. Here, we study the transition from tropical to temperate climates in the grass subfamily Pooideae, which dominates the northern temperate grass floras. Specifically, we investigate the role of climate cooling in diversification.  Location Global, temperate regions  Time period Late Cretaceous-Cenozoic  Major taxa The grass subfamily Pooideae  Methods We date a comprehensive Pooideae phylogeny and test for the impact of paleoclimates on diversification rates. Using ancestral state reconstruction, we investigate if Pooideae ancestors experienced frost and winter. To locate the area of origin of Pooideae we perform biogeographical analyses.  Results We estimated a late Cretaceous origin of the Pooideae (66 million years ago (Mya)), and all major clades had already diversified at the Eocene-Oligocene transition climate cooling (34 Mya). Climate cooling was a probable driving force of Pooideae diversification. Pooideae likely evolved in mountainous regions of southwestern Eurasia in a temperate niche experiencing frost, but not long winters.  Main conclusion Pooideae originated in a temperate niche and experienced cold temperatures and frost long before the expansion of temperate biomes after the Eocene-Oligocene transition. This suggests that the Pooideae ancestor had adaptations to temperate climate and that extant Pooideae grasses share responses to low temperature stress in Pooideae. Throughout the Cenozoic falling temperatures triggered diversification. However, complex mechanisms for enduring strongly seasonal climate with long, cold winters most likely evolved independently in lower taxonomic lineages. Our findings provide insight into how adaptations to historic changes in chill and frost exposure influence distribution of plant diversity today.

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Successive evolutionary steps drove Pooideae grasses from tropical to temperate regions

Cited by 32 publications

References 80 publications

Evolution of Cold Acclimation and Its Role in Niche Transition in the Temperate Grass Subfamily Pooideae

Evolution of Cold Acclimation and Its Role in Niche Transition in the Temperate Grass Subfamily Pooideae

The grass subfamily Pooideae: Cretaceous–Palaeocene origin and climate‐driven Cenozoic diversification

The grass subfamily Pooideae: late Cretaceous origin and climate-driven Cenozoic diversification

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