Resolution of sex chromosomes in waterhemp and Palmer amaranth

The genus Amaranthus L. includes nine dioecious species: Amaranthus acanthochiton J.D. Sauer, Amaranthus arenicola I.M. Johnson, Amaranthus australis (A. Gray) J.D. Sauer, Amaranthus cannabinus (L.) J.D. Sauer, Amaranthus floridanus (S. Watson) J.D. Sauer, Amaranthus tuberculatus (Moq.) J.D. Sauer, Amaranthus greggii S. Watson, Amaranthus watsonii Standley, and Amaranthus palmeri S. Watson that are native to North America and grouped into the subgenus Acnida (L.) Aellen ex K.R. Robertson. Two of the dioecious species, A. tuberculatus (waterhemp) and A. palmeri (Palmer amaranth), are agronomically important weeds that have evolved resistance to herbicides from several modes of action and have spread beyond their native ranges. A strategy that has been proposed for the management of these weedy dioecious species to complement existing tools (such as herbicide technology, crop rotation, seedbank depletion etc.) is a genetic control, whereby sex ratios could be biased towards one gender (e.g., males) and the genetic factors involved are inherited in a non-Mendelian pattern via a gene drive system. The depletion of the other gender (i.e., females) required for outcrossing over multiple generations thus results in population collapse. Adopting such a genetic control strategy however requires a comprehensive understanding of the factors and mechanisms responsible for sex determination as well as evolutionary relationships among the dioecious species. While previous studies confirmed males were the heterogametic sex and identified several candidate genes within putative sex-determining regions, as well as differentially expressed genes between males and females with likely role in sex determination, the contiguity of these sex-determining regions and the genomic architecture of the chromosome (colloquially referred to as the “sex chromosome”) that harbors the sex determinants remain poorly understood. Chapter 1 includes a brief overview of genome sequencing and assembly of sex chromosomes; evolution and mechanisms of sex determination in plants; and the genetics of dioecy evolution within the Amaranthus genus. Chapter 2 explores the relationships among the dioecious amaranths using Mash distances, as well as the conservation of candidate genes previously identified within the A. palmeri and A. tuberculatus sex-determining regions in other dioecious amaranths. The results of this study confirmed Sauer’s taxonomic ordering of the dioecious amaranths, which was based on comparative morphology, and indicated two possible independent origins of dioecy evolution within the Amaranthus genus. Chapter 3 further explores the relationships among the dioecious amaranths utilizing their complete chloroplast genomes. Although some species relationships were consistent with the previous Mash tree, the chloroplast phylogeny indicates that the relationships of the A. australis + A. cannabinus lineage to the other dioecious species remains unclear and showed that A. palmeri and A. watsonii are more genetically related than previously reported. We also provide a framework for investigating evolutionary relationships among the amaranths and demonstrate that the use of complementary phylogenetic approaches coupled with proper species identification could be very informative in examining the complex evolutionary history of the genus. Chapter 4 focuses on the sequencing, assembly, phasing, and annotation of the A. tuberculatus genome as well as identification of the sex chromosomes within the assembly. We present a chromosome-level haplotype-resolved genome of A. tuberculatus and report a contiguous ~32.8 Mb region near the middle of chromosome 1 as the sex-determining region. We show that the sex chromosome in A. tuberculatus likely originated from the fusion of two ancestral chromosomes. Chapter 5 describes the sequencing, assembly, and annotation of A. palmeri, A. retroflexus, and A. hybridus genomes, and the identification of the sex chromosomes in the A. palmeri assembly. Here, we present a chromosome-level phased genome of three Amaranthus species (A. palmeri, A. retroflexus, and A. hybridus) and report a contiguous ~2.84 Mb region at the distal end of chromosome 3 of A. palmeri as the sex-determining region. Finally, Chapter 6 provides concluding remarks on sex determination within the Amaranthus genus and future directions on finding the candidates genes and mechanisms involved.

Name thesis:degree_name

Ph.D.

Level thesis:degree_level

Dissertation

Discipline thesis:degree_discipline

Crop Sciences

Grantor

University of Illinois at Urbana-Champaign

Year dc:date

2024

Author dc:creator

• Raiyemo, Damilola Alex

Contributors dc:contributor

• Tranel, Patrick J
• Hager, Aaron G
• Studer, Anthony J
• Burgess, Steven J

• Waterhemp
• Palmer Amaranth
• Genome Assembly
• Sex-determining Regions
• Dioecy
• Chromosomal Fusion
• Amaranthus Species

Statement dc:rights

• Copyright 2024 Damilola Alex Raiyemo

Language dc:language

en, eng

Handle dc:identifier

https://hdl.handle.net/2142/125682

OAI record oai:identifier

https://www.ideals.illinois.edu/oai-pmh?verb=GetRecord&metadataPrefix=etdms&identifier=oai%3Awww.ideals.illinois.edu%3A2142%2F125682