Ricardo A. Chávez Montes, Anna Haber, Jeremy Pardo, Robyn F. Powell, Upendra K. Divisetty, Anderson T. Silva, Tania Hernández-Hernández, Vanildo Silveira, Haibao Tang, Eric Lyons, Luis Rafael Herrera Estrella, Robert VanBuren, and Melvin J. Oliver

PNAS February 1, 2022 119 (5) e2118886119

Figure: Sporobolus pyramidalis; Poaceae family.

Significance

This is a significant sister group contrast comparative study of the underpinning genomics and evolution of desiccation tolerance (DT), a critical trait in the evolution of land plants. Our results revealed that the DT grass Sporobolus stapfianus is transcriptionally primed to tolerate a dehydration/desiccation event and that the desiccation response in the DT S. stapfianus is distinct from the water stress response of the desiccation-sensitive Sporobolus pyramidalis. Our results also show that the desiccation response is largely unique, indicating a recent evolution of this trait within the angiosperms, and that inhibition of senescence during dehydration is likely critical in rendering a plant desiccation tolerant.

Abstract

Desiccation tolerance is an ancient and complex trait that spans all major lineages of life on earth. Although important in the evolution of land plants, the mechanisms that underlay this complex trait are poorly understood, especially for vegetative desiccation tolerance (VDT). The lack of suitable closely related plant models that offer a direct contrast between desiccation tolerance and sensitivity has hampered progress. We have assembled high-quality genomes for two closely related grasses, the desiccation-tolerant Sporobolus stapfianus and the desiccation-sensitive Sporobolus pyramidalis. Both species are complex polyploids; S. stapfianus is primarily tetraploid, and S. pyramidalis is primarily hexaploid. S. pyramidalis undergoes a major transcriptome remodeling event during initial exposure to dehydration, while S. stapfianus has a muted early response, with peak remodeling during the transition between 1.5 and 1.0 grams of water (gH₂O) g⁻¹ dry weight (dw). Functionally, the dehydration transcriptome of S. stapfianus is unrelated to that for S. pyramidalis. A comparative analysis of the transcriptomes of the hydrated controls for each species indicated that S. stapfianus is transcriptionally primed for desiccation. Cross-species comparative analyses indicated that VDT likely evolved from reprogramming of desiccation tolerance mechanisms that evolved in seeds and that the tolerance mechanism of S. stapfianus represents a recent evolution for VDT within the Chloridoideae. Orthogroup analyses of the significantly differentially abundant transcripts reconfirmed our present understanding of the response to dehydration, including the lack of an induction of senescence in resurrection angiosperms. The data also suggest that failure to maintain protein structure during dehydration is likely critical in rendering a plant desiccation sensitive.

See https://www.pnas.org/content/119/5/e2118886119

Fig. 5. ELIPs tandem duplication in S. stapfianus and ELIP gene abundance in leaf tissues. (A) Microsynteny of two ELIP tandem arrays is shown in S. stapfianus. ELIPs are shown in red, other genes are shown in gray, and syntenic homeologs between the scaffolds are denoted by gray connections. (B) The number of ELIPs in sequenced Chloridoideae grasses (E. tef, S. stapfianus, S. pyramidalis, E. coracana, O. thomaeum, and Z. mays) is plotted. The two desiccation-tolerant grasses are denoted in red. (C) Log₂-transformed gene abundance (TPM) of the 30 ELIPs in S. pyramidalis and 65 ELIPs in S. stapfianus across each replicate of the leaf desiccation time courses.