RESEARCH-PGR: Dissecting the dynamic evolution of paralogs in shaping trait variation across the Solanum Pan-Genome

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The growing population and climate extremes are threatening food security. Agriculture is largely based on a few major crops, and revolutionary technologies in genome sequencing and CRISPR genome engineering are accelerating their improvement. These technologies can also improve “orphan” crops, which are not widely cultivated or studied but have the potential to increase the diversity and resilience of food production. Orphan crops are related to major crops, allowing translation of knowledge between them. However, orphan crops lack research tools, and an even greater challenge is determining whether specific genetic mutations that benefitted major crops can be engineered to improve traits similarly in orphan crops. This is because gene sequence and function change as species evolve, especially among genes that become duplicated, which is common in plants. This project will take advantage of the nightshade family – a source of many major and orphan crops, such as eggplant, pepino, and tomato – to study how duplicated genes evolve and affect agricultural traits in related species. Combining genome sequencing and CRISPR will reveal sequence diversity among thousands of duplicated genes and enable improved predictability in engineering genes and traits across species. This project will train young scientists with a focus on diversity and inclusion, as well as promote public understanding of genome engineering in plant biology through a community science program on orphan crops. Finally, new curricula and research opportunities for undergraduate students at a small liberal arts college will broaden participation and training of underrepresented groups in the plant sciences.This project will exploit advances in large-scale reference genome sequencing, gene co-expression analyses, and CRISPR genome editing to dissect how paralog diversification impacts species-specific phenotypes in a genus of both fundamental and applied importance. Fifty Solanum species, including 16 orphan crops, will be sequenced to establish a Solanum Pan-Genome with telomere-to-telomere reference assemblies, providing a foundation for genus-wide comparative genomics and functional genetics. Computational approaches based on genomics data will be developed for precise assembly and comparison of complex genomes, and identification and classification of paralogs and their relationships based on their variants and expression patterns. Simultaneously, transformation protocols and genome editing will be developed and deployed for an array of Solanum to test how paralogs impact genotype-to-phenotype relationships within and between species. By focusing on major domestication gene families and the adaptation and productivity traits they control, this synergistic work will provide both a new understanding of paralog diversification in evolution and a more robust translation of agriculturally relevant genotype-to-phenotype relationships to orphan crops. Beyond a valuable community resource of Solanum reference genomes, expression data, and CRISPR lines for plant researchers and breeders, this multidisciplinary project will result in new tools, resources, and principles that will enable the study and engineering of other taxa and traits of significance to both plant biology and crop improvement.This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.