Cellulose synthase machinery in thickened primary cell walls of celery collenchyma via prizm of transcriptome analysis.

Cellulose biosynthesis remains one of the most fascinating topics in plant science. Although the main components involved in cellulose biosynthesis have been characterized, significant gaps remain in our understanding of these processes. Celery (Apium graveolens L.) collenchyma, a mechanical tissue composed of elongating cells with thickened primary cell walls (PCWs), serves as an excellent model for studying cell wall formation and modification. This tissue exemplifies both the shared features of PCWs and the unique properties specific to collenchyma. In celery, cellulose synthase A genes (CESAs) and their potential cofactors, which represent the “core” components of cellulose biosynthesis, have been identified and annotated. In collenchyma, six CESA isoforms associated with PCW biosynthesis (AgrCESA1-A, AgrCESA1-B, AgrCESA3-A, AgrCESA6L-A, AgrCESA6L-B, and AgrCESA6L-C) show elevated expression levels. These genes are part of a distinct coexpression network, while those linked to secondary cell wall (SCW) biosynthesis (AgrCESA4, AgrCESA7, and AgrCESA8) cluster within a separate coexpression network. Among the PCW-related CESA isoforms, transcript levels vary considerably: AgrCESA3-A exhibits the highest expression, whereas AgrCESA6L-C shows the lowest. At the mature stage, the expression levels of most AgrCESA genes decrease across all tissues. However, the relative ratios of transcript abundance among different AgrCESA subunits within the cellulose synthase complex remain relatively stable, regardless of tissue type or developmental stage. The structural peculiarities of the collenchyma cell wall, which enable simultaneous loosening and thickening, may result from both the direct intensification of the entire cellulose biosynthesis pathways and an increase in the transcript abundance of specific cofactors.