Evidence for recent evolution of cold tolerance in grasses suggests current distribution is not limited by (low) temperature

Humphreys, Aelys M.; Linder, H. Peter

doi:10.1111/nph.12244

Cited by 39 publications

(46 citation statements)

References 60 publications

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“…Although climate is commonly considered the major determinant of species distribution, it may well be that other biotic and abiotic factors confound the link between a specific climate parameter and the fundamental niche (Soberon & Arroyo‐Peña, ). A study of the realized niche of cold tolerance in the southern temperate grass subfamily Danthonioideae indeed underestimated the fundamental niche (Humphreys & Linder, ). However, Humphreys and Linder () also showed that species experiencing cold temperatures in their native range showed a higher survival rate in a growth experiment of overwintering capacity, indicating a close correlation between realized niche and physical tolerance to frost.…”

Section: Discussionmentioning

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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Section: Discussionmentioning

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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“…) but only to a limited extent because no clear relation between cold tolerance evolution and the distribution range has been established (Skálová et al . ; Humphreys & Linder ). Through evolutionary history, more angiosperms have radiated into freezing environments through three key cold tolerance mechanisms: decreasing the hydraulic conduit diameter, becoming deciduous and shortening their life form (Zanne et al .…”

Section: Introductionmentioning

confidence: 99%

“…). However, the current understanding of this evolutionary mechanism is insufficient to explain the rapid cold differentiation that is observed among plant populations (Humphreys & Linder ; Leiblein‐Wild et al . ; Zanne et al .…”

Section: Introductionmentioning

confidence: 99%

ICE1 demethylation drives the range expansion of a plant invader through cold tolerance divergence

Xie

Liu

et al. 2015

Molecular Ecology

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Cold tolerance adaption is a crucial determinant for the establishment and expansion of invasive alien plants into new cold environments; however, its evolutionary mechanism is poorly understood. Crofton weed (Ageratina adenophora), a highly invasive alien plant, is continuously spreading across subtropical areas in China, north-eastward from the first colonized south-western tropical regions, through cold tolerance evolution. Close relations between the cold tolerance levels of 34 populations, represented by 147 accessions, and the latitude, extreme lowest temperature, coldest month average temperature, and invasion period have provided direct insight into its cold tolerance divergence. A comparative study of the CBF pathway, associated with the cold tolerance enhancement of cold-susceptible CBF1-transgenic plant, among four geographically distinct crofton weed populations revealed that the CBF pathway plays a key role in the observed cold tolerance divergence. Four epialleles of the cold response regulator ICE1 ranged from 66 to 50 methylated cytosines, representing a 4.4% to 3.3% methylation rate and significantly corresponding to the lowest to highest cold tolerance levels among these different populations. The significant negative relation between the transcription levels of the primary CBF pathway members, except for CBF2, and the methylation levels among the four populations firstly demonstrates that the demethylation-upregulated transcription level of CBF pathway is responsible for this evolution. These facts, combined with the cold tolerance variation and methylation found among three native and two other introduced populations, indicate that the ICE1-demethylated upregulation of cold tolerance may be the underlying evolutionary mechanism allowing crofton weed to expand northward in China.

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“…Despite its tropical origins, a few grass clades have successfully diversified in temperate environments Humphreys and Linder, 2013). In particular, the diversification of Pooideae grasses in the northern hemisphere coincides with a period of major global cooling that peaked during the Eocene-Oligocene boundary 34 to 33.5 million years ago (Zachos et al, 2001;Mannion et al, 2014).…”

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confidence: 99%

Evidence for an Early Origin of Vernalization Responsiveness in Temperate Pooideae Grasses

et al. 2016

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The ability of plants to match their reproductive output with favorable environmental conditions has major consequences both for lifetime fitness and geographic patterns of diversity. In temperate ecosystems, some plant species have evolved the ability to use winter nonfreezing cold (vernalization) as a cue to ready them for spring flowering. However, it is unknown how important the evolution of vernalization responsiveness has been for the colonization and subsequent diversification of taxa within the northern and southern temperate zones. Grasses of subfamily Pooideae, including several important crops, such as wheat (Triticum aestivum), barley (Hordeum vulgare), and oats (Avena sativa), predominate in the northern temperate zone, and it is hypothesized that their radiation was facilitated by the early evolution of vernalization responsiveness. Predictions of this early origin hypothesis are that a response to vernalization is widespread within the subfamily and that the genetic basis of this trait is conserved. To test these predictions, we determined and reconstructed vernalization responsiveness across Pooideae and compared expression of wheat vernalization gene orthologs VERNALIZATION1 (VRN1) and VRN3 in phylogenetically representative taxa under cold and control conditions. Our results demonstrate that vernalization responsive Pooideae species are widespread, suggesting that this trait evolved early in the lineage and that at least part of the vernalization gene network is conserved throughout the subfamily. These results are consistent with the hypothesis that the evolution of vernalization responsiveness was important for the initial transition of Pooideae out of the tropics and into the temperate zone.

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Evidence for recent evolution of cold tolerance in grasses suggests current distribution is not limited by (low) temperature

Cited by 39 publications

References 60 publications

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

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

ICE1 demethylation drives the range expansion of a plant invader through cold tolerance divergence

Evidence for an Early Origin of Vernalization Responsiveness in Temperate Pooideae Grasses

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