Genomic insights into the recent chromosome reduction of autopolyploid sugarcane Saccharum spontaneum

Abstract

S. spontaneum is a founding Saccharum species that contributes stress resistance to the genetic background of modern sugarcane cultivars. Here, we have assembled the autopolyploid S. spontaneum Np-X genome with ancestral form into 40 pseudo-chromosomes in 10 homologous groups, revealing the recent chromosome reduction and polyploidization that occurred in Saccharum. The paleo-duplicated chromosomal pairs exhibit functional redundancy in Saccharum and underwent ssion followed by fusion accompanied by centromeric spreading around 0.80 million years ago (Mya) before evolving into their current forms with basic chromosome numbers x = 9 and x = 8 in S. spontaneum, likely in a stepwise manner. WGDs occurred independently in Saccharum species around 1.5 Mya. Highly diverse chromatin structures exist among homologous chromosomes despite their high collinearity, and the re-structuring of NpChr5 and NpChr8 might have suppressed switching of chromatin structure from inactive to active. Resequencing of 116 sugarcane accessions elucidated that the S. spontaneum originated from North India and that the basic chromosome numbers x = 8, x = 9, and x = 10 originated independently, indicating that recent chromosome reduction rather than polyploidization has driven the adaptive evolution of Saccharum. Our study provides genomic resources and suggests new directions for accelerating sugarcane improvement and advances our knowledge of the evolution of auto-polyploids.

Reconstruction of karyotypic evolution in Saccharum spontaneum species by comparative oligo-FISH mapping

“…The two published Sa. spontaneum (x = 8 and x = 10) genomes also show that almost all chromosomes were metacentric or submetacentric, which was consistent with our cytology results [ 28 , 29 ]. According to normal logic, all chromosomes were metacentric type in Sa.…”

“…spontaneum split from Sa. officinarum about 1.6 Mya [ 28 ], while the Sa. officinarum has been considered to be domesticated from Sa.…”

“…Sugarcane is one of the most important economic crops with an annual value of US$90 billion and provides 80% of the world's sugar and 40% of ethanol [28]. Published genomic studies show that sugarcane and sorghum genomes are mostly collinear in the genic regions, sharing a common ancestor about 8-9 million years ago [29][30][31].…”

“…To date, no natural diploid sugarcane has been found, and sorghum (2n = 2x = 20) can be tentatively regarded as the hypothetical diploid sugarcane ancestor type. Saccharum spontaneum is a founding Saccharum species with wide variation in chromosome numbers (2n = 4x = 40 to 2n = 8x = 128) [28]. Previous studies have demonstrated that Saccharum spontaneum species exhibits three basic chromosome numbers, x = 8, x = 9 or x = 10 [28,29,[32][33][34].…”

Genome-wide characterization of cys-tathionine-β-synthase domain-containing proteins in sugarcane reveals their role in defense responses under multiple stressors

“…Modern sugarcane cultivars with an allo-autopolyploid genome contain chromosomes from S. officinarum (80%) and S. spontaneum (10%) ( D’Hont et al, 1996 ), but the characteristics of stress response, disease resistance, and regeneration ability of these cultivars are derived from S. spontaneum ( Garsmeur et al, 2018 ). To better understand features of the sugarcane genome, two reference genome sequences from the S. spontaneum clones AP85-441 ( Zhang et al, 2018 ) and Np-X ( Zhang et al, 2022 ) were assembled at the chromosome level, while three draft genome sequences from hybrid genotypes R570 ( Garsmeur et al, 2018 ), SP80-3280 ( Souza et al, 2019 ), and CC01-1940 ( Trujillo-Montenegro et al, 2021 ) were assembled at a non-chromosome level. These sugarcane genome sequences, particularly in AP85-441 and Np-X, are convenient for exploring how resistance genes are related to various stress responses in sugarcane.…”