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Tolerance of desiccation and UV radiation in mosses of the genus Syntrichia (Pottiaceae), from genomes to ecology


An environmental stressor, UV radiation is a potentially important selective factor in ecosystems with high solar exposure. Natural solar radiation can be damaging to plants, including to important components of plant metabolism. In addition to protecting tissues from dangerous levels of radiation, maintaining access to sufficient water is also an important problem for terrestrial organisms to solve. Common in drylands, the moss genus Syntrichia contains some of the most desiccation-tolerant plants known. Desiccation tolerance (DT), defined as the ability to equilibrate to dry air and resume normal metabolic activity after rehydration, allows organisms to survive dry periods and limit metabolic activity to periods of moisture availability. These resilient mosses can lose most of their cellular water, remain quiescent for decades, and begin photosynthesizing and recovery immediately upon rehydration.

In this dissertation, I explore molecular and physiological responses of two Syntrichia species to UV radiation in a variety of field, laboratory, and combined experiments to gain insight on the adaptive mechanisms allowing these organisms to thrive in dryland habitats. The first chapter is an eco-physiology study that focuses on the effects of natural levels of UV radiation on photosynthesis. The second and third chapters are controlled laboratory experiments that explore plasticity in the response to different levels of UV radiation and, in the third, how the response might interact with desiccation.

In Chapter 1, I used an in-situ field experiment to uncover the effects of natural and reduced levels of UV on maximum PSII quantum efficiency (Fv/Fm), relative abundance of photosynthetic pigments and antioxidants, and on the transcriptome in the desiccation-tolerant desert moss Syntrichia caninervis. I tested the hypotheses that: (1) natural S. caninervis plants undergo sustained thermal quenching of light (non-photochemical quenching; NPQ) while desiccated and after rehydration, (2) a reduction of UV will result in improved recovery of Fv/Fm, but (3) one year of UV removal will de-harden plants and increase vulnerability UV damage to photosynthetic efficiency. All field-collected plants had extremely low Fv/Fm after initial rehydration but recovered over eight days in lab-simulated winter conditions. UV-filtered plants had lower Fv/Fm during recovery, higher concentrations of photoprotective pigments and antioxidants such as zeaxanthin and tocopherols, and lower concentrations neoxanthin and chlorophyll b than plants exposed to near natural UV levels. Natural S. caninervis undergoes sustained NPQ that takes days to relax and for efficient photosynthesis to resume. Reduction of solar UV radiation adversely effects recovery of Fv/Fm following rehydration.

In Chapter 2, I investigated the genetic underpinnings to acute broadband UV exposure in S. caninervis and S. ruralis, using a comparative transcriptomics approach. In particular, I aimed to uncover whether UV protection is physiologically plastic and induced by UV exposure with the following questions: (1) what is the timeline of changes in the transcriptome with acute UV exposure in these two species, (2) what genes are involved in the acute UV response, and (3) how do the two species differ in their transcriptomic response to UV. There was no strong transcriptomic response with 10 minutes of UV exposure in either S. ruralis or S. caninervis and relatively small number of significant genes at 30 minutes, suggesting a physiologically constitutive, rather than plastic or acclimated, protection to UV radiation. Yet, there was remarkable differences between the two species after 30 minutes, including nearly twice as many significant genes (including two early light-inducible protein genes) for S. caninervis than for S. ruralis. Many significant genes in both species were involved in oxidation-reduction, suggesting oxidative stress. Late embryogenesis abundant genes were also involved in both species in response to UV, possibly suggesting their role in UV tolerance or as evidence of cross-talk for desiccation tolerance. Taken together, the results of this study suggest potential UV-induced responses that might have roles outside of desiccation tolerance, and that the response to UV is different in these two species, perhaps a reflection of adaption to different environmental conditions.

In Chapter 3, I conducted a fully factorial experiment comparing the separate and combined effects of two levels of UV radiation and a desiccation treatment in S. ruralis and S. caninervis to uncover the nature of correlation between DT and UV tolerance. When exposure to one type of stressor confers or enhances protection to another type it can be due to either “cross-tolerance” (overlap in the mechanism of protection for two or more types of stressors) or “cross-talk” (when there is overlap in signaling pathways in response to different stressors but separate mechanisms of protection). I tested the following hypotheses: (1) There is cross-talk in the genetic underpinnings of the UV and desiccation response pathways for S. caninervis. (2) S. ruralis will instead show a pattern of cross-tolerance with UV and desiccation stresses, evidenced by distinct transcriptomic responses to the two stressors but overlap in metabolomic responses. I found evidence of both cross-talk and cross tolerance in both species, but with nuanced differences in their response to the individual and combined stresses. In particular, I found support for the hypothesis of cross-talk in the UV and desiccation response pathway for S. caninervis, evidenced by shared transcriptomic response to the two stressors with no significant interaction. I also found key transcripts and metabolites that shed light on the mechanisms of tolerance to these two stressors, both individually and combined. Notably, phenolics were involved in the UV response at both the transcriptomic and metabolomic levels, though with differences between species and interactions with desiccation, indicating potential for a UV sunscreen and for cross-talk and cross-tolerance in these species. Furthermore, there were candidate UVT genes and metabolites that were not induced by UV in S. caninervis but were in S. ruralis, supporting the hypothesis that S. ruralis has a more plastic, acclimatable UV response than S. caninervis, and that these differences are predictable by their unique interaction with these stressors as poikilohydric organisms. The genetic and metabolomic findings of this study can be directly used to test hypotheses and further elucidate mechanisms of UV protection and VDT in these stress-tolerant plants and a greater understanding of mechanism can lead to development of engineering technologies to improve crop plants’ ability to withstand combined stresses.

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