The evolution of desiccation tolerance in angiosperm plants: a rare yet common phenomenon

Abstract

Abstract. In a minute proportion of angiosperm species, rehydrating foliage can revive from airdryness or even from equilibration with air of~0% RH. Such desiccation tolerance is known from vegetative cells of some species of algae and of major groups close to the evolutionary path of the angiosperms. It is also found in the reproductive structures of some algae, moss spores and probably the aerial spores of other terrestrial cryptogamic taxa. The occurrence of desiccation tolerance in the seed plants is overwhelmingly in the aerial reproductive structures; the pollen and seed embryos. Spatially and temporally, pollen and embryos are close ontogenetic derivatives of the angiosperm microspores and megaspores respectively. This suggests that the desiccation tolerance of pollen and embryos derives from the desiccation tolerance of the spores of antecedent taxa and that the basic pollen/embryo mechanism of desiccation tolerance has eventually become expressed also in the vegetative tissue of certain angiosperm species whose drought avoidance is inadequate in microhabitats that suffer extremely xeric episodes. The protective compounds and processes that contribute to desiccation tolerance in angiosperms are found in the modern groups related to the evolutionary path leading to the angiosperms and are also present in the algae and in the cyanobacteria. The mechanism of desiccation tolerance in the angiosperms thus appears to have its origins in algal ancestors and possibly in the endosymbiotic cyanobacteria-related progenitor of chloroplasts and the bacteria-related progenitor of mitochondria. The mechanism may involve the regulation and timing of the accumulation of protective compounds and of other contributing substances and processes.

Orthodox Seeds and Resurrection Plants: Two of a Kind?

“…An analysis of two orphan genes from C. plantagineum (a Cys-rich rehydrationresponsive protein1 gene [CpCRP1] and an early dehydration-responsive protein1 gene [CpERD1]) involved in the dehydration/rehydration cycle suggested recent, family-specific evolution of these two genes (Giarola et al, 2015b). This finding suggests that different genetic architectures underlie the resurrection phenotype, and it supports the notion that independent evolutionary events led plants to reacquire vegetative DT (Gaff and Oliver, 2013).…”

“…Later, during the evolution of angiosperms, resurrection plants reacquired DT in their vegetative tissues through myriad genetic changes in at least 13 separate lineages (Oliver et al, 2005;Porembski, 2011;Gaff and Oliver, 2013). These lineages correspond to the angiosperm families containing resurrection species (Oliver et al, 2005;Gaff and Oliver, 2013). Interestingly, these families are not in a linear phylogenetic sequence from one to the other, and except for Myrothamnaceae and Velloziaceae, only a small portion of the species in each family possess vegetative DT (Gaff and Oliver, 2013).…”

“…These lineages correspond to the angiosperm families containing resurrection species (Oliver et al, 2005;Gaff and Oliver, 2013). Interestingly, these families are not in a linear phylogenetic sequence from one to the other, and except for Myrothamnaceae and Velloziaceae, only a small portion of the species in each family possess vegetative DT (Gaff and Oliver, 2013).…”

“…Later, during the evolution of angiosperms, resurrection plants reacquired DT in their vegetative tissues through myriad genetic changes in at least 13 separate lineages (Oliver et al, 2005;Porembski, 2011;Gaff and Oliver, 2013). These lineages correspond to the angiosperm families containing resurrection species (Oliver et al, 2005;Gaff and Oliver, 2013).…”

Regulatory network analysis reveals novel regulators of seed desiccation tolerance in Arabidopsis thaliana

“…At least 13 independent cases of evolution (or reevolution) of vegetative DT occurred in the angiosperms and 1 in gymnosperms (21). The independent reevolution of vegetative DT in different clades of the angiosperms suggests that despite being a quite complex process, both vegetative and seed DT might be controlled…”