Meiotic abnormalities in sugarcane (Saccharum spp.): Evidence for peri- and paracentric inversions

Abstract

The modern cultivars of sugarcane (Saccharum spp.) are highly polyploid and accumulate aneuploidies due to their history of domestication, genetic improvement and interspecific hybrid origin involving the domesticated sweet species S. officinarum ('noble cane') and the wild S. spontaneum, both with an evolutionary history of polyploidy. The first hybrids were backcrossed with S. officinarum, and selection from progenies in subsequent generations established the genetic basis of modern cultivars. Saccharum genome complexity has inspired several molecular studies that have elucidated aspects of sugarcane genome constitution, architecture and cytogenetics. Herein, we conducted a comparative analysis of the meiotic behavior of representatives of the parentals S. officinarum and S. spontaneum, and the commercial variety, SP80-3280. S. officinarum, an octoploid species, exhibited regular meiotic behavior. In contrast, S. spontaneum and SP80-3280 exhibited several abnormalities from metaphase I to the end of division. We reported and typified, for the first time, the occurrence of peri- and paracentric inversions. Using in-situ hybridization techniques, we were able to determine how pairing association occurred at diakinesis and, in particular, the chromosome composition of SP80-3280. Our findings have implications for sugarcane genetic mapping, genomics, and for studies on resynthesized polyploids.

First investigation into the genetic control of meiosis in sugarcane

“…It is an establishing autopolyploid (Van Drunen & Friedman, 2022), with several cytotypes and basic chromosome numbers ( x ) equal to 10, 9, and 8 (Piperidis & D'Hont, 2020), being x = 8 the most common. Its meiosis is irregular with approximately 52% of cells exhibiting abnormalities and up to two univalent are seen in diakinesis (Oliveira et al., 2023). Therefore, it is reasonable to speculate that meiotic cells require a higher expression of ZIP4 for regulation of meiotic synapsis.…”

“…In the same study, using genomic in situ hybridization (GISH), we also determined the origin of lagging chromosomes, mostly from S. spontaneum and from interspecific recombination events, suggesting that there is coordinated, non‐random meiotic chromosome segregation. In all, our previous studies revealed the existence of mechanisms that regulate meiosis, and they require further in‐depth investigation (Oliveira et al., 2023; Vieira et al., 2018).…”

“…Current varieties have complex genomes and vary in chromosome number ( 2n = 110–130). According to molecular cytogenetic analysis, S. officinarum and S. spontaneum account, respectively, for 75–85% and 15–25% of their chromosomes, plus ~10% of recombinants, produced by synapsis and crossover (CO) involving homoeologous chromosomes (Cuadrado, 2004; D'Hont et al., 1996; Oliveira et al., 2023; Piperidis et al., 2010; Piperidis & D'Hont, 2020).…”

“…From a meiotic point of view, classical cytogenetic analyses suggest that both parental species and interspecific hybrids predominantly form bivalents (Burner, 1991; Nair, 1975; Price, 1963a, 1963b; Suzuki, 1941). Recently, our group performed a comparative analysis of meiotic behavior in representatives of S. officinarum (clone Caiana Fita) and S. spontaneum (clone SES205A), as well as the Brazilian variety SP80‐3280 (Oliveira et al., 2023), which exhibited several abnormalities, whereas the behavior of S. officinarum , an ‐ octoploid species, was found to be regular. Using centromeric probes and fluorescent in situ hybridization (FISH), we were able to enumerate the bivalents that prevailed, although in S. spontaneum and SP80‐3280, one or two univalents were found in diakinesis.…”

Meiotic chromosome behavior in >i<Saccharum>/i< species, including the Brazilian variety SP80-3280

“…The two latter exhibited several abnormalities, including delayed chromosomes, from metaphase I to the end of the division, while the S. officinarum clone showed regular behavior. In this study, we visualized the presence of dicentric chromosomes, and a pericentric inversion that was particularly evidenced by a detailed pachytene analysis (Oliveira et al 2022).…”