As we look towards an increasingly dry future, it is critical that we develop a deep understanding of how organisms thrive in arid biomes in order to protect, utilize, and sustainably manage arid lands for maximal productivity. These efforts should include building a fundamental understanding of natural adaptations to water scarcity, which span diverse life histories, morphologies, and physiologies. My research is focused on resurrection plants, a remarkable group of phylogenetically diverse species that represent some of the most water-stress tolerant plants on earth. These plants can recover from extreme desiccation by entering a state of quiescence where nearly all metabolic activity ceases. Untangling the genetic, cellular, and organismal mechanisms of desiccation tolerance will offer key insights into how life can survive without water, and could enable breakthrough innovations in agriculture, astrobiology, anhydro-preservation, and beyond. Despite the important insights into anhydrobiosis that resurrection plants will provide, many species are understudied due to their rarity, the remote and rugged conditions of their native habitats, and challenges associated with experimental manipulation of non-model organisms.
Evolutionary genomics of desiccation tolerance
Desiccation tolerance is, in many ways, the epitome of drought tolerance and resurrection plants can survive typically lethal levels of water loss. Resurrection plants are not a monophyletic group–they span ~500 million years of evolution divergence with representatives in diverse families of angiosperms, pteridophytes, lycophytes, and bryophytes (Figure 1). Desiccation tolerance likely arose independently in these lineages, perhaps convergently, using deeply conserved pathways. Resurrection plants are not randomly distributed across the landscape and typically form symbiotic communities on rocky outcrops (ruwari) that are inhospitable to most other plants. The richest diversity of known resurrection plants can be found in southern Africa, where they experience sustained drought for months at a time during the dry season. Despite their phylogenetic diversity and unique life histories, a core set of metabolic, physiological, and structural changes have been observed in response to drying across many lineages. The repeated and recurrent evolution of desiccation tolerance, conserved cellular responses, and overlapping ecological distributions suggest this trait evolved convergently through rewiring similar pathways. Taken together, resurrection plants provide an excellent comparative framework to identify the origin, genetic basis, and diversity of desiccation tolerance strategies. Using comparative genomics coupled with time-ordered gene expression, physiology, and metabolomic datasets we are building integrative models of diverse desiccation tolerance strategies and distinguish among core and species-specific mechanisms in over a dozen diverse species.
Figure 1. The striking morphological and phylogenetic diversity of resurrection plants. These species span ~500 million years of evolution and divergence, yet they all share the striking ability to survive complete desiccation. The co-occur in tight association on ruwari and other rocky habitats in tropical and subtropical regions of the world.
Figure 2. Conceptual overview of desiccation tolerance. A) contrasting selective pressure leads to local adaptation. B) Whole plant morphological and physiological mechanisms. C) Changes induced during drying. D) Cellular and genetic responses.
Natural variation in desiccation tolerance within a single species
Surveying intraspecific variation is a powerful way to identify discrete genetic differences underlying traits of interest, as opposed to the conserved biochemical, physiological, or network level changes identified via cross-species comparisons. 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 natural variation in resurrection plants. Consequently, multiple knowledge gaps exist regarding genetic diversity, plasticity, and genotype by environment interactions in resurrection plants.
My current work investigates the patterns and consequences of intraspecific variation in desiccation tolerance in three divergent resurrection species, each expected to represent different evolutionary paths to desiccation tolerance: Microchloa caffra, Myrothamnus flabellifolia, and Pallaea calomelanos. Each of these species is widely distributed and expected to exhibit phenotypic variation across their native range. We are collecting and characterizing small diversity panels to test if intraspecific variation in desiccation tolerance exists along these environmental gradients. Cross-scale datasets spanning ecology, physiology, metabolism, and gene expression will then be collected to identify discrete differences among populations and ecotypes of each species.
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.
EXPOSING INEQUITIES in SCIENCE
My research is also directly related to diversifying plant science, and I hope to contribute to shifting paradigms and improving equity in academia more broadly. I believe that fostering a diverse, thriving discipline with empowered researchers across continents, regardless of socioeconomic status, will yield the greatest potential to meet the economic, social, and evolutionary challenges facing twenty-first-century science. In addition to my collaborative research program in South Africa, I am working to critically dissect the forces that perpetuate inequality in academia using the tools of data science.
Our recent paper on representation and participation in plant genomics has sparked an important conversation about the legacy of colonialism and its implications for science today. We showed that stark participation biases exist in plant genomics with researchers in the global south (particularly Africa and South America) being significantly underrepresented. Over 75% of published genomes have been led by researchers in affluent nations in central Europe, the USA, and China, and in many cases, researchers from these areas sequenced exotic plants native to the Global South with minimal collaborative efforts.
Building on this work, I am continuing to leverage the tools of data science to describe global patterns, participation gaps, and inequities in scientific research. Along with my collaborators, we build, curate, and analyze large-scale genomic and bibliometric datasets, to address fundamental questions about the global landscape of participation in science, identify areas of underrepresentation, and offer suggestions towards building a more inclusive discipline. Our current project investigates nearly 300,000 plant science papers to understand what demographic and socioeconomic factors impact research output and academic currency. Again, our analyses reveal striking global participation imbalances (Figure 3), a lack of intercontinental collaborations (Figure 4), persistent gender biases (Figure 5), and an overwhelmingly eurocentric power structure.
Figure 4. Global distribution of plant science authors from 2000-2021, scaled by the number of publications from each location.
Figure 4. Global collaboration network of plant science research. Circles represent publications that did not involve an intercontinental collaboration. Arrows represent cross-continental collaborations and are directed from corresponding author to co-author.
Figure 5. Stagnant gender bias over the past two decades. The proportion of authors with female names over the last 20 years is plotted for each of the eight geographical regions investigated.
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 sexual 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.
Figure 6. Life cycle of Marchantia inflexa.
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.