Biased mutations and gene losses underlying diploidization of the tetraploid broomcorn millet genome

Abstract

SUMMARY Broomcorn millet (Panicum miliaceum L.) is one of the earliest domesticated crops, and is a valuable resource to secure food diversity and combat drought stresses under the global warming scenario. However, due to the absence of extant diploid progenitors, the polyploidy genome of broomcorn millet remains poorly understood. Here, we report the chromosome‐scale genome assembly of broomcorn millet. We divided the broomcorn millet genome into two subgenomes using the genome sequence of Panicum hallii, a diploid relative of broomcorn millet. Our analyses revealed that the two subgenomes diverged at ~4.8 million years ago (Mya), while the allotetraploidization of broomcorn millet may have occurred about ~0.48 Mya, suggesting that broomcorn millet is a relatively recent allotetraploid. Comparative analyses showed that subgenome B was larger than subgenome A in size, which was caused by the biased accumulation of long terminal repeat retrotransposons in the progenitor of subgenome B before polyploidization. Notably, the accumulation of biased mutations in the transposable element‐rich subgenome B led to more gene losses. Although no significant dominance of either subgenome was observed in the expression profiles of broomcorn millet, we found the minimally expressed genes in P. hallii tended to be lost during diploidization of broomcorn millet. These results suggest that broomcorn millet is at the early stage of diploidization and that mutations likely occurred more on genes that were marked with lower expression levels.

A high-quality, phased genome assembly of broomcorn millet reveals the features of its subgenome evolution and 3D chromatin organization

“…We also verified that this method could successfully reconstruct the K and N subgenomes of switchgrass AP13 ( Lovell et al., 2021 ) ( Supplemental Figure 3 ). Our results were consistent with another newly released broomcorn millet genome (Jinshu7) ( Sun et al, 2022 ) in which the two subgenomes were phased using P. hallii as a diploid reference ( Supplemental Figure 4 ). Three major translocation events were found between the two subgenomes of broomcorn millet ( Figure 1 C), which were supported by canonical Hi-C interaction of the involved chromosomes ( Supplemental Figure 5 ).…”

Pangenome of water caltrop reveals structural variations and asymmetric subgenome divergence after allopolyploidization

“…2a ; Tables S9 and S18 , see online supplementary material), suggesting this TE-rich subgenome may experience more gene losses, and eventually become a recessive subgenome due to ongoing gene loss [ 43 ]. Similar patterns have been observed in the genome of tetraploid broomcorn millet ( Panicum miliaceum ), one of the earliest domesticated crops [ 44 ]. Besides, PAVs were found to have a greater impact on homologous gene expression in TnAt than in TnBt ( Fig.…”

A complete reference genome of broomcorn millet

“…We compared the length distribution of genes among the AJ8, maize 12 , sorghum (GCF_000003195.3) 39 , LM_1 8 , and Jinshu7 7 and found similar patterns (Fig. 3a ).…”

“…Stringtie (v 1.2.2) 37 and TransDecoder (v 5.7.1) ( https://github.com/TransDecoder/TransDecoder ) were employed to assemble the transcripts and identify candidate coding regions into gene models (Stringtie-set). Homologous genomes from seven plants, including rice (T2T-NIP) 10 , maiz e (T2T Mo17) 12 , A. thaliana (Col-PEK) 38 , sorghum (GCA_000003195.3) 39 , pearl millet (Tift23D2B1-P1-P5) 40 , foxtail millet (GCA_000263155.2) 41 , and two previous versions of broomcorn millet (Jinshu7: GCA_026771285.1; Longmi4: GCA_002895445.3) 7 , 9 were downloaded and used as queries to search against the AJ8 T2T assembly using GeMoMa (v 1.9) 42 . These homology predictions were referred to as “Homology-set”.…”

“…Broomcorn millet has an allotetraploid genome consisting of 36 (2n = 4x = 36) chromosomes 6 . Although four chromosome-level of broomcorn millet, Jinshu7 7 , LM_v1 8 , LM_v2 9 , and Pm_0390 8 , have been made available, there are still missing segments within the genome due to the presence of highly repetitive sequences clustered across the genome, particularly in the telomere and centromere regions. In recent years, T2T and gap-free genomes have been successfully obtained in various important crops, including rice 10 , barley 11 , and maize 12 .…”