Biology subjects

Purugganan, M. D.

Publications and source records attributed to Purugganan, M. D..

6 recordsLinked to original sources

bioRxiv2025

Environment-dependent selection impacts heritable developmental stability and trait canalization in rice

Canalization, or the maintenance of trait values regardless of environmental or genetic variability, is fundamentally important for maintaining developmental stability. While this concept was described decades ago, we still know relatively little about how canalization is influenced by environmental stress, how it is shaped by natural selection, and the genetic underpinnings of canalization. In this study, we examined natural selection on microenvironmental canalization in rice (Oryza sativa) in wet and dry field conditions. We measured developmental stability in genetically identical replicates obtained from geographically widespread Indica and Japonica rice accessions, providing precise estimates of canalization in thousands of plants. We found that drought stress decreased canalization, showing that stress can increase instability. We also found evidence that canalization can evolve, given that canalization of several traits was heritable and under selection. We further uncovered specific genes underlying canalization, with genetic mapping and functional genetic experiments showing that the bZIP transcription factor-encoding gene OsTGA5/rTGA2.3, which is part of a module that balances stress response and plant growth, regulates canalization of several traits in an environment-dependent manner. At a genome-wide scale, canalization was associated with lower gene expression stochasticity at an earlier life stage, indicating that expression variation can reduce canalization and increase instability. Trait canalization was also positively correlated to temperature at accessions source environments, suggesting that selection on canalization can vary among environments. Overall, our study provides novel insights into the molecular genetic basis of environmental differences in developmental stability and how it might be shaped by selection. SignificanceMechanisms stabilizing organismal development in response to genetic mutations or environmental stressors (canalization) have been reported for numerous animals and plants, but their underlying genetic basis and whether they may be shaped by selection remain unclear. Here, we report patterns of drought-induced trait decanalization in populations of rice (Oryza sativa) grown in field environments. We determined that trait canalization is heritable and can evolve separately from trait means. We identified the gene OsTGA5, part of a regulatory module shaping trade-offs between growth and stress responses, as impacting trait canalization. Plants with less noisy gene expression and evolving in warmer environments display greater developmental stability, contributing to the notion that canalization in rice may be adaptive.

evolutionary biology↗

bioRxiv2024

System genomics of salinity stress response in rice

Populations can adapt to stressful environments through changes in gene expression. However, the fitness effect of gene expression in mediating stress response and adaptation remains largely unexplored. Here, we use an integrative field dataset obtained from 780 plants of Oryza sativa ssp. indica (rice) grown in a field experiment under normal or moderate salt stress conditions to examine selection and evolution of gene expression variation under salinity stress conditions. We find that salinity stress induces increased selective pressure on gene expression. Further, we show that trans-eQTLs rather than cis-eQTLs are primarily associated with rices gene expression under salinity stress, potentially via a few master-regulators. Importantly, and contrary to the expectations, we find that cis-trans reinforcement is more common than cis-trans compensation which may be reflective of rice diversification subsequent to domestication. We further identify genetic fixation as the likely mechanism underlying this compensation/reinforcement. Additionally, we show that cis- and trans-eQTLs are under balancing and purifying selection, respectively, giving us insights into the evolutionary dynamics of gene expression variation. By examining genomic, transcriptomic, and phenotypic variation across a rice population, we gain insights into the molecular and genetic landscape underlying adaptive salinity stress responses, which is relevant for other crops and other stresses.

systems biology↗

bioRxiv2021

Evolutionary systems biology reveals patterns of rice adaptation to drought-prone agro-ecosystems

Rice was domesticated around 10,000 years ago and has developed into a staple for half of humanity. The crop evolved and is currently grown in stably wet and intermittently dry agro-ecosystems, but patterns of adaptation to differences in water availability remain poorly understood. While previous field studies have evaluated plant developmental adaptations to water deficit, adaptive variation in functional and hydraulic components, particularly in relation to gene expression, has received less attention. Here, we take an evolutionary systems biology approach to characterize adaptive drought resistance traits across roots and shoots. We find that rice harbors heritable variation in molecular, physiological, and morphological traits that is linked to higher fitness under drought. We identify modules of co-expressed genes that are associated with adaptive drought avoidance and tolerance mechanisms. These expression modules showed evidence of polygenic adaptation in rice subgroups harboring accessions that evolved in drought-prone agro-ecosystems. Fitness-linked expression patterns had predictive value and allowed us to identify the drought-adaptive nature of optimizing photosynthesis and interactions with arbuscular mycorrhizal fungi. Taken together, our study provides an unprecedented, integrative view of rice adaptation to water-limited field conditions.

plant biology↗

bioRxiv2019

Genomic history and ecology of the geographic spread of rice

Rice (Oryza sativa) is one of the worlds most important food crops. We reconstruct the history of rice dispersal in Asia using whole-genome sequences of >1,400 landraces, coupled with geographic, environmental, archaeobotanical and paleoclimate data. We also identify extrinsic factors that impact genome diversity, with temperature a leading abiotic factor. Originating [~]9,000 years ago in the Yangtze Valley, rice diversified into temperate and tropical japonica during a global cooling event [~]4,200 years ago. Soon after, tropical rice reached Southeast Asia, where it rapidly diversified starting [~]2,500 yBP. The history of indica rice dispersal appears more complicated, moving into China [~]2,000 yBP. Reconstructing the dispersal history of rice and its climatic correlates may help identify genetic adaptation associated with the spread of a key domesticated species.\n\nOne sentence summaryWe reconstructed the ancient dispersal of rice in Asia and identified extrinsic factors that impact its genomic diversity.

evolutionary biology↗

bioRxiv2019

Genome assembly and characterization of a complex zfBED-NLR gene-containing disease resistance locus in Carolina Gold Select rice with Nanopore sequencing

BackgroundLong-read sequencing facilitates assembly of complex genomic regions. In plants, loci containing nucleotide-binding, leucine-rich repeat (NLR) disease resistance genes are an important example of such regions. NLR genes make up one of the largest gene families in plants and are often clustered, evolving via duplication, contraction, and transposition. We recently mapped the Xo1 locus for resistance to bacterial blight and bacterial leaf streak, found in the American heirloom rice variety Carolina Gold Select, to a region that in the Nipponbare reference genome is rich in NLR genes.\n\nResultsToward identification of the Xo1 gene, we combined Nanopore and Illumina reads to generate a high-quality genome assembly for Carolina Gold Select. We identified 529 full or partial NLR genes and discovered, relative to the reference, an expansion of NLR genes at the Xo1 locus. One NLR gene at Xo1 has high sequence similarity to the cloned, functionally similar Xa1 gene. Both harbor an integrated zfBED domain and near-identical, tandem, C-terminal repeats. Across diverse Oryzeae, we identified two sub-clades of such NLR genes, varying in the presence of the zfBED domain and the number of repeats.\n\nConclusionsWhole genome sequencing combining Nanopore and Illumina reads effectively resolves NLR gene loci, providing context as well as content. Our identification of an Xo1 candidate is an important step toward mechanistic characterization, including the role(s) of the zfBED domain. Further, the Carolina Gold Select genome assembly will facilitate identification and exploitation of other useful traits in this historically important rice variety.

plant biology↗

bioRxiv2018

The complex geography of domestication of the African rice Oryza glaberrima

While the domestication history of Asian rice has been extensively studied, details of the evolution of African rice remains elusive. The inner Niger delta has been suggested as the center of origin but molecular data for its support are lacking. Here, we present the most comprehensive analysis to date on the evolutionary and domestication history of African rice. By analyzing whole genome re-sequencing data from 282 individuals in domesticated African rice Oryza glaberrima and its progenitor O. barthii, we hypothesize a non-centric domestication origin for African rice. Our analyses show geographically based population structure in O. glaberrima, as well as significant evidence of admixture between genetic groups. Furthermore, we have evidence that the previously hypothesized O. barthii progenitor populations in West Africa have evolutionary signatures similar to domesticated rice and carried causal domestication mutations, suggesting those progenitors may actually represent feral wild-domesticated hybrid rice. Demography modeling suggested the inland O. glaberrima had a protracted period of bottlenecking that preceded the coastal population by 800-1,800 years. Phylogeographic analysis of genes involved in the core domestication process suggests that the origins of causal domestication mutations could be traced to wild progenitors in multiple different locations in West and Central Africa. Based on our evidence, we hypothesize O. glaberrima was not domesticated from a single centric location but was rather a diffuse process where multiple regions contributed key alleles for different domestication traits.\n\nAuthor SummaryFor many crops it is not clear how they got domesticated from their wild progenitors. Transition from a wild to domesticated state required a series of genetic changes, and studying the evolutionary origin of these domestication-causing mutations are key to understanding the domestication origins of a crop. Moreover, population relationships within a crop holds insight into the evolutionary history of domestication and whether there was gene flow between different genetic groups. In this study, we investigate the domestication history of Oryza glaberrima, a rice species that was domesticated in West Africa independently from the Asian rice species O. sativa. Using genome-wide data from a large sample of domesticated and wild African rice samples we did not find evidence that supported the established domestication model for O. glaberrima--a single domestication origin. Rather, our evidence suggests the domestication process for African rice was initiated in multiple regions of West Africa, caused potentially by the local environmental and cultivation preference of people. Admixture between different genetic groups had facilitated the exchange and spread of core domestication mutations. Hence domestication of African rice was a multi-regional process.

evolutionary biology↗