ToColdlyGo Where No Grass has Gone Before: A Multidisciplinary Review of Cold Adaptation in Poaceae

Abstract

The grass family Poaceae is among the largest and most successful plant families, both ecologically and economically. It covers a wide geographic, climatic, and ecological range and contains many of the world's most important crops including wheat, barley, rice, maize, and sorghum, as well as many forage and biofuel species. Both wild and cultivated grasses are diverse in areas that regularly experience cold and freezing as well as high seasonality, harsh winters, and short growing seasons. Grasses growing in these environments have evolved an arsenal of strategies to tolerate or resist cold stress, or to escape the cold by phenological adjustments. Here, we review the current knowledge of cold adaptations in grasses synthesising across the disciplines of stress physiology, genetics, metabolomics, ecology, and evolution, in both wild and cultivated species. Specifically, we explore what is known about molecular and physiological cold stress responses, how these might have evolved and their role in shaping diversification and distribution patterns of grasses. We argue that integrating insights from multiple disciplines will further our understanding of cold adaptation.

The cold-drought tolerance trade-off in temperate woody plants constrains range size, but not range filling

“…To summarize, while we recognize that adaptations to very low temperatures are complex, and involve a combination of avoidance and tolerance strategies together with acclimation (Schubert et al , 2020), we argue that large range sizes at the cold tolerant end of the trade-off axis is made viable because of the deciduous habit in temperate woody species. In this instance, stress avoidance is more important as an asset than stress tolerance.…”

Major niche transitions in Pooideae correlate with variation in photoperiodic flowering and evolution of CCT domain genes

“…2 ) suggests that the dual photoperiod–temperature induction of flowering long known from winter Pooideae cereals ( Heide, 1994 ) was a key step toward colonizing newly expanding temperate climates. Recent dating of the grasses ( Burke et al , 2016 ; Gallaher et al , 2019 ; Schubert et al , 2019a ) places the origin of Pooideae at the transition between the Cretaceous and Paleocene, 60–70 million years ago (Mya), at a time when mean temperatures were relatively high ( Zachos et al , 2001 ) and seasonality in temperature relatively low ( Archibald et al , 2013 ). Biogeographic studies suggest a Eurasian origin for Pooideae ( Bouchenak-Khelladi et al , 2010 ), and a recent reconstruction of the ancestral niche of Pooideae suggests that its ancestor experienced frost ( Schubert et al , 2019a ), consistent with a cold micro-habitat origin, possibly in montane Eurasia.…”

“…Recent dating of the grasses ( Burke et al , 2016 ; Gallaher et al , 2019 ; Schubert et al , 2019a ) places the origin of Pooideae at the transition between the Cretaceous and Paleocene, 60–70 million years ago (Mya), at a time when mean temperatures were relatively high ( Zachos et al , 2001 ) and seasonality in temperature relatively low ( Archibald et al , 2013 ). Biogeographic studies suggest a Eurasian origin for Pooideae ( Bouchenak-Khelladi et al , 2010 ), and a recent reconstruction of the ancestral niche of Pooideae suggests that its ancestor experienced frost ( Schubert et al , 2019a ), consistent with a cold micro-habitat origin, possibly in montane Eurasia. Together, these results imply that Pooideae was already to some degree adapted to the cool, seasonal northern climates that developed after the Eocene–Oligocene (E–O) boundary 34 Mya ( Strömberg, 2011 ), and that the early origins of vernalization responsiveness and long-day flowering played crucial roles in the shift of Pooideae from tropical to temperate regions.…”

“…Genomic DNA was extracted from leaf material using the DNeasy Plant MiniKit (Qiagen, Valencia, CA, USA), following the manufacturer’s protocol. We obtained sequences for three DNA plastid regions matK , ndhF , and rbcL , using custom Pooideae-specific primers ( Schubert et al , 2019a ; Supplementary Table S2 ). PCR was performed on a Tetrad 2 Thermal Cycler (Bio-Rad, Hercules, CA, USA) and a Mastercycler ep Gradient Thermal Cycler (Eppendorf, Hamburg, Germany) using JumpStart REDTaq ReadyMix (Sigma-Aldrich, St. Louis, MO, USA) and standard conditions with 58 °C annealing and 2 min extension.…”

“…Similar to angiosperms as a whole ( Hochuli and Feist-Burkhardt, 2013 ; Mannion et al , 2014 ), the grass family evolved when the terrestrial Earth was largely tropical ( Burke et al , 2016 ; Gallaher et al , 2019 ; Schubert et al , 2019a ), suggesting that the ancestor would either have flowered under short days or been daylength neutral ( Preston and Fjellheim, 2020 ). Indeed, of the ~12 000 extant grass species ( Soreng et al , 2015 ), the majority remain in the tropics, with only a couple of major subfamilies—Danthonioideae and Pooideae—dominating southern and northern temperate regions, respectively ( Edwards and Smith, 2010 ; Visser et al , 2014 ; Schubert et al , 2020 ).…”