First investigation into the genetic control of meiosis in sugarcane

Author(s)

Soares, Nina Reis ; Costa, Zirlane Portugal ; Marques, Joao Paulo Rodrigues ; Garsmeur, Olivier ; Carneiro, Monalisa Sampaio ; Vitorello, Claudia Barros Monteiro ; D'Hont, Angelique ; Vieira, Maria Lucia Carneiro

• Document type: Journal article
• Source: Plant Journal; v. 118, n. 6, p. 14-pg., 2024-03-25.

Abstract

The sugarcane (Saccharum spp.) genome is one of the most complex of all. Modern varieties are highly polyploid and aneuploid as a result of hybridization between Saccharum officinarum and S. spontaneum. Little research has been done on meiotic control in polyploid species, with the exception of the wheat Ph1 locus harboring the ZIP4 gene (TaZIP4-B2) which promotes pairing between homologous chromosomes while suppressing crossover between homeologs. In sugarcane, despite its interspecific origin, bivalent association is favored, and multivalents, if any, are resolved at the end of prophase I. Thus, our aim herein was to investigate the purported genetic control of meiosis in the parental species and in sugarcane itself. We investigated the ZIP4 gene and immunolocalized meiotic proteins, namely synaptonemal complex proteins Zyp1 and Asy1. The sugarcane ZIP4 gene is located on chromosome 2 and expressed more abundantly in flowers, a similar profile to that found for TaZIP4-B2. ZIP4 expression is higher in S. spontaneum a neoautopolyploid, with lower expression in S. officinarum, a stable octoploid species. The sugarcane Zip4 protein contains a TPR domain, essential for scaffolding. Its 3D structure was also predicted, and it was found to be very similar to that of TaZIP4-B2, reflecting their functional relatedness. Immunolocalization of the Asy1 and Zyp1 proteins revealed that S. officinarum completes synapsis. However, in S. spontaneum and SP80-3280 (a modern variety), no nuclei with complete synapsis were observed. Importantly, our results have implications for sugarcane cytogenetics, genetic mapping, and genomics. Our work provides insights into the genetic control of meiosis in sugarcane (Saccharum spp.), a man made polyploid and fertile plant of interspecific constitution. Inspired by the discoveries of the Ph1 locus, which harbors the ZIP4 gene in wheat, we identified this meiotic gene in both parental species and in two current sugarcane varieties. We analyzed both gene and protein sequence conservation, protein domains, and predicted the 3D-protein structure. We also investigated the level of ZIP4 expression in different sugarcane tissues. Like its role in wheat, ZIP4 seems to promote pairing between homologous chromosomes while suppressing crossover between homeologs in Saccharum. Using immunocytology, we were able to determine synaptonemal complex polymerization during prophase I, using Asy1 and Zyp1 sugarcane specific antibodies, revealing synapsis defects in all genotypes except Saccharum officinarum, a parental species with regular meiotic behavior. (AU)

• FAPESP's process: 20/07741-0 - Chromosome constitution, meiotic behavior and genetic control of synapsis in the sugarcane variety SP80-3280
• Grantee: Maria Lúcia Carneiro Vieira
• Support Opportunities: Regular Research Grants
• FAPESP's process: 19/07838-6 - Unraveling the genome of Passiflora organensis: a reference for Passifloraceae and evolutionary studies
• Grantee: Zirlane Portugal da Costa
• Support Opportunities: Scholarships in Brazil - Post-Doctoral