Exogenous auxin-induced rapid modulation of herbaceous peony stem straightness: insights into transient cell wall metabolism responses.

Abstract

Key message: Exogenous IAA applying within 32 days after herbaceous peony bud germination induces a 6-h transient stem change: first bending then upright. This process correlates with the degradation of cell wall substances like cellulose and pectin. Herbaceous peony (Paeonia lactiflora) holds a growing presence in the cut flower market. A vital criterion for selecting cut herbaceous peonies is the uprightness of their stems, which is largely determined by cell wall materials (CWMs). Our previous study indicated that applying indole-3-acetic acid (IAA) during the development process could enhance the stem straightness of herbaceous peonies at the flowering stage. Interestingly, in certain development phases, after IAA application, the stems were observed to first bend and then regain an upright position within hours (transient changes), yet the underlying mechanism remains unclear. This study aimed to identify the stages during which these transient changes occur and elucidate the role of CWMs in terms of their contents, enzyme activities, metabolites, and gene expression. The results showed that IAA-induced transient changes were most prevalent in the first three stages. The accumulated cellulose, pectin, and lignin in the IAA-treated group were consumed as the stem regained their upright position. Cinnamyl-alcohol dehydrogenase, β-glucosidase, and pectin methylesterase played key degradation roles. Combined metabolome and transcriptome analyses revealed that differential metabolites and differentially expressed genes were enriched in pathways such as glycolysis/gluconeogenesis, xylan biosynthesis process, secondary cell wall biogenesis, and lignin catabolism. The cellulose synthesis gene CESA2, decomposition gene CEL5, and pectin decomposition gene At1g48100 deserved further investigation. This study provides support for clarifying the mechanism by which IAA regulates stem uprightness of P. lactiflora and serves as a reference for selection and cultivation of herbaceous peony cut flowers.