With climate change models predicting increased variation in global weather patterns, including frequent and intense droughts, both ecological stability and food security are threatened. In order to protect the communities and industries that rely on plant productivity, it is critical that we work towards strategies to enhance water-stress tolerance in plants. These efforts should include building a fundamental understanding of the many natural adaptations to water scarcity, which span diverse life histories, morphologies, and physiologies. This diversity represents a valuable repository of information that can be mined to gain insight into the biology of water-stress tolerance. My research is focused on resurrection plants, which represent some of the most water-stress tolerant plants on earth. These plants can recover from nearly complete desiccation (below an absolute water content of -100M Pa) by entering a state of quiescence where (nearly) all metabolic activity ceases. The advantages of this trait, if applied to crops in drought prone and marginal sites, cannot be overstated. Although desiccation tolerance has fascinated scientists for decades, the complexity and variability of the phenotype has limited our ability to distinguish the key features and genes regulating this ability.
Evolutionary genomics of desiccation tolerance
Desiccation tolerance is an ancestral trait that facilitated territorialization by early plants. The phylogenetic distribution of extant resurrection plants (Figure 1) suggests that tolerance was lost (or suppressed) in the common ancestor of vascular plants, and re-evolved convergently in a subset of lineages. Despite extensive phylogenetic and morphological diversity, resurrection plants typically co-occur in specific habitat types, suggesting that environmental selection has been a strong driving force in the retention and re-evolution of desiccation tolerance. In fact, it is common to find species spanning ~400 million years of divergence growing as complex intertwined communities, making this an ideal system to study convergent evolution
Understanding the evolutionary history of desiccation tolerance will provide critical insight into the underlying molecular mechanisms of tolerance. If desiccation tolerance re-evolved convergently across vascular plants, then it is likely that different mechanisms were repurposed in diverse lineages to give rise to the same phenotype, some of which may be more or less efficient, effective, or applicable in particular contexts. My research uses a combination of ecological, molecular, and computational to distinguish among the multiple mechanisms of desiccation tolerance. This work has the potential to transform our understanding of desiccation tolerance by identifying core vs distinct aspects of tolerance.
Desiccation tolerant lineages (highlighted in blue) are mapped onto the land plant phylogeny. The trait distribution suggests that ancestral tolerance was retained in early diverging lineages (indicated by the widespread occurrence across bryophytes), that desiccation tolerance was lost (or suppressed) in the common ancestor of vascular plants, and then re-evolved convergently in a unique subset of lineages (indicated by the presumptive multiple independent origins of desiccation tolerance across vascular plant lineages).
Natual varation in desiccation tolerance in the South African resurrection plant Myrothamnus flabellifolia
The extent of intraspecific variability in desiccation tolerance is largely uncharacterized, but is likely significant, similar to other highly convergent adaptations to water deficit such as CAM and C4 photosynthesis. Many desiccation tolerant angiosperms are widely distributed across sub-Saharan Africa, Asia, Australia, and South America with stark differences in elevation, precipitation, and temperature across their native range. Presumably, levels of desiccation tolerance vary in concordance, but this has rarely been tested, limiting our understanding of adaptive processes and population level dynamics in resurrection plants. My recent work indicates that desiccation tolerance can vary between individuals of the same species in specific contexts challenging the belief that it is a fixed trait.
Currently I am working to establish a diversity panel of the unique and understudied resurrection plant Myrothamnus flabellifolia, which will be leveraged to pinpoint genetic and physiological variation giving rise to elevated desiccation tolerance. The study is integrated across organizational scales, addressing ecological, physiological, and genomic components of desiccation tolerance. We have established field sites across South Africa to monitor long-term ecological dynamics of M. flabellifolia. These data will be paired with genomic resources, allowing us to investigate the impact of natural diversity and genetic variation on adaptive phenotypes.
In addition to being desiccation tolerant, M. flabellifolia produces a robust profile of secondary compounds with important medicinal applications. Our work includes a plan to engage local communities in the sustainable cultivation of M. flabellifolia for medicinal purposes.
BRYOPHYTE ECOLOGY and EVOLUTION
Genomics and sex chromosome evolution of Marchantia inflexa
Bryophytes (mosses, liverworts, and hornworts) are living representatives of early diverging land plant lineages and they provide an important landmark for comparative phylogenetics. Building a fundamental understanding of genomic patterns can be readily accomplished by working with bryophytes because of their small genomes, many of which contain comparatively few paralogous duplications of regulatory genes. Interestingly, bryophytes harbor a high proportion of dioecious species. Nearly half of all extant mosses, and approximately two-thirds of liverworts are dioecious, and this provides an ideal system in which to untangle the complex biology of sex ula dimporphism and sex determination in plants. Additionally, the haploid gametophyte is the dominant life stage in bryophytes, and this offers a unique perspective on the evolution of sex-linked genes, as the female (U) and male (V) sex chromosomes are present at the same copy number (1N) as autosomal chromosomes for the majority of the organism’s life cycle and are subject to haploid selection. We took advantage of these characteristics to gain insight into how haploid selection shapes sex chromosome evolution and to identify genomic signatures of stress tolerance, both of which inform our understanding of early plant evolution.
Eco-physiology of desiccation tolerance in Marchantia inflexa
My PhD work focused on characterizing the ecophysiology of desiccation tolerance in the tropical liverwort Marchantia inflexa. We took advantage natural variation in desiccation tolerance among populations to gain deeper insight into the causes and consequences of sexual dimorphisms in desiccation tolerance. Understanding sexual dimorphisms in stress tolerance is important because these dimorphisms can drive spatial segregation of the sexes, lead to biased population sex ratios, and may ultimately reduce sexual reproduction and population persistence. In general, we found that that plants were increasingly desiccation tolerant in drier sites, due to a combination of local adaptation and plasticity. Complex sexual dimorphisms were also detected, which likely contribute to population level dynamics.
Plant-microbe interactions have major implications for agricultural productivity, ecosystem function, and nutrient cycling. However, information on the establishment, diversity, and function of the plant microbiome remains limited, especially for non-vascular plants. In an effort to fill this knowledge gap, we described the bacteriome of the tropical liverwort Marchantia inflexa. We found that the bacteriome is abundant, diverse, and shows similarities with other non-vascular plant lineages. On the basis of known microbial functions, our analyses suggest that the specific taxonomic assemblages of bacteria detected in different sites may serve functional roles; allowing plants to better acclimate to their local environment. Our data also suggest that sex differences in the bacteriome may correspond to subtle differences in the morphology of the sexes.
Currently, we (mostly Caylyn Railey, a brilliant undergraduate working on the project) are testing if a functional link exists between the plant bacteriome and desiccation tolerance. Caylyn is growing multiple lines of M. inflexa under aseptic culture and characterizing subsequent changes desiccation tolerance.