Haplotype-phased genomes elucidate genetic architecture of environmental adaptation and domestication traits in Silphium

Authors: SOUZA, RENAN - Hudsonalpha Institute For Biotechnology; CLEVENGER, JOSHUA - Hudsonalpha Institute For Biotechnology; JENKINS, JERRY - Hudsonalpha Institute For Biotechnology; KORANI, WALID - Hudsonalpha Institute For Biotechnology; SCHMUTZ, JEREMY - Hudsonalpha Institute For Biotechnology; GRIMWOOD, JANE - Hudsonalpha Institute For Biotechnology; PLOTT, CHRISTOPHER - Hudsonalpha Institute For Biotechnology; HANDLEY, LORI - Hudsonalpha Institute For Biotechnology; WEBBER, JENELL - Hudsonalpha Institute For Biotechnology; BOSTON, LORI - Hudsonalpha Institute For Biotechnology; BRANDVAIN, YANIV - University Of Minnesota; MILLER, ALLISON - Donald Danforth Plant Science Center; WOELTJEN, STELLA - Donald Danforth Plant Science Center; RUBIN, MATTHEW - St Louis University; SMITH, KEVIN - University Of Minnesota; Hulke, Brent; NASTASI, LOUIS - University Of Iowa; MURRELL, EBONY - Savanna Institute; TURNER, KATHRYN - The Land Institute; HARKESS, ALEX - Hudsonalpha Institute For Biotechnology; VAN TASSEL, DAVID - The Land Institute

Submitted to: Research Square
Publication Type: Pre-print Publication
Publication Acceptance Date: 2/6/2026
Publication Date: 2/6/2026
Citation: Souza, R., Clevenger, J., Jenkins, J., Korani, W., Schmutz, J., Grimwood, J., Plott, C., Handley, L.5., Webber, J., Boston, L.B., Brandvain, Y., Miller, A., Woeltjen, S., Rubin, M., Smith, K., Hulke, B.S., Nastasi, L.F., Murrell, E., Turner, K., Harkess, A., Van Tassel, D. 2026. Haplotype-phased genomes elucidate genetic architecture of environmental adaptation and domestication traits in Silphium. Research Square. https://doi.org/10.21203/rs.3.rs-8753360/v1.
DOI: https://doi.org/10.21203/rs.3.rs-8753360/v1

Interpretive Summary: As agriculture faces increasing pressure from changing environmental conditions, there is an urgent need for more resilient crop options. This research highlights the potential of Silphium, a North American prairie plant, to serve as a new type of perennial crop. Unlike traditional annual crops that must be replanted every year, these native species have deep, permanent root systems that allow them to thrive during droughts and effectively prevent soil erosion, making them a natural defense against environmental instability. While these plants are naturally hardy, they have historically been difficult to farm because their complex genetic makeup made traditional breeding too slow and unpredictable. This study represents a major technological breakthrough by successfully mapping the entire DNA sequence of two key Silphium species. By decoding these massive genomes, researchers have created a "genetic roadmap" that identifies the specific genes responsible for critical farming traits, such as seed size, flowering time, and overall yield. Ultimately, this genomic toolkit allows scientists to fast-track the domestication of a wild plant into a high-performing commercial crop. For the United States, this means more stable food supplies, healthier soil, and a more competitive agricultural economy that can withstand the extreme weather conditions of the future.

Technical Abstract: Agriculture will face major challenges in the upcoming decades. In addition to feeding a growing population, production must be sustainable and resilient against the extreme conditions being imposed by climate change. Native perennial crops can be an important option to ensure that the agricultural systems are resilient against biotic and abiotic stresses and have a reduced footprint on the environment. Wild plants could contribute a wide range of adaptations to diversify and improve the functionality of agricultural systems. However, wild species are difficult to manage, harvest and breed with classical approaches due to reproductive constraints, such as self-incompatibility, and genomic complexities, such as large repetitive genomes and polyploidy. Overall these factors have been a barrier to the development of native perennial crops, but with advances in genomic technologies, this is about to change. The possibility of assembling complex genomes and generating markers quickly and cost effectively means that wild plants can be domesticated and bred faster with marker assisted selection similarly to major crops. Here we report the assembly of reference genomes for Silphium integrifolium Michx. and Silphium perfoliatum L. These two perennial species are native to North American prairies and are known for their tolerance to drought and the ability to reduce soil erosion due to their deep root structure. The haplotype-phased genome assembly resulted in 7 chromosomes per haplotype with a genome size of 7.6 Gb for S. integrifolium and 7.5 Gb for S. perfoliatum, and BUSCO scores ranging from 97% to 98%. The genomes exhibited a newly observed putative helical structure preserved during meiotic interphase with a loop circumference of 43 Mb. This structure has been hypothesized to be necessary to maintain genome integrity in organisms with large chromosomes. The gene content in S. integrifolium and S. perfoliatum was estimated to be 44,653 and 43,390, respectively. We performed target-sequencing at the gene regions in 16 species to reconstruct the phylogeny of Silphium. We recovered the two previously accepted subgenera, Composita and Silphium, but found several species to be nonmonophyletic, highlighting the need for further taxonomic and sequencing work on the genus. In addition to target sequencing, we implemented a combinatorial approach with low-pass whole genome sequencing to generate 449K SNPs. We developed the Silphium association panel (SAP) with 258 accessions and performed a spatial ancestry analysis to understand the population structure and the first genome-wide association studies for the genus and provided an overview of 7 traits related to domestication and 3 traits for environmental adaptation. The spatial ancestry analysis revealed the existence of two ancestral populations in the central US with clinal variation in the East-West gradient. The GWAS revealed 77 loci explaining from 1% to 44.7% of the phenotypic variance. Notably, the genes silint01g06242 (alpha/beta hydrolase) and silint01g14554 (MATE family efflux transporter) accounted for 51.5% of the variance for seed number per capitulum and the latter was also associated with capitulum receptacle diameter and ray floret count. A variant in the gene silint04g01657 (ACR4-related protein) was strongly with ray floret count (22% of the variance). The genes silint01g14003 (PR5 Thaumatin family protein) and silint01g11956 (MATE family efflux transporter) were attributed to 12% and 11% of the variance in the number of stems, respectively. For flowering time, a SNP in the gene silint03g07644 (Nodulin Homeobox - NDX) explained 10.3% of the variance. For the average seed mass, 10 QTLs were identified, together accounting for 57.9 % of the variance in the population. For the aridity index, 3 QTLs explained 46.9% of the variance and for the heat index, eight QTLs explained 34