Regulatory control of orchestrated silk elongation moderated by sugar metabolism, phytohormone signalling and secondary metabolite dynamics

BACKGROUND AND AIMS: As the stigma of the female flower in maize, silks emerge sequentially from ear base to apex, potentially causing a barren ear tip. The aim of this study was to reveal the underlying regulatory mechanisms in coordinating the elongation of a cohort of silks on an ear. METHODS: Morphological, physiological, metabolic and transcriptional investigations were performed on silks from basal, middle and apical regions of an ear at the initial (T1), rapid elongation (T2) and silking (T3) stages, respectively. KEY RESULTS: Silk extension rate and length declined progressively from ear base to apex, correlated with decreased hexose availability owing to lower sucrose supply, weaker sucrose decomposition and the gradient in phytohormone deposition. Further comparative analyses on silk metabolomics and transcriptomics between the three stages and three positions identified the stage-specific and position-specific genes and metabolites. The elongation of silks at the three positions involves common pathways, including sugar and amino acid depletion, secondary metabolite biosynthesis and phytohormone responses. Stage-specific pathways indicated that nucleic acid metabolism was predominant at T1, carbohydrate and energy metabolism at T2, and defence metabolism at T3. Position-specific pathways highlighted the earlier biosynthesis of secondary metabolites in basal silks, and delayed phytohormone signalling, starch and sucrose metabolism and mitogen-activated protein kinase signalling in apical silks. At T3, silk senescence progressed from ear base to apex by having more severe sugar depletion, salicylic/jasmonic acid deposition and active brassinosteroid/abscisic acid synthesis. CONCLUSIONS: The sequential silk elongation on an ear is coordinated collectively by competition of assimilates, phytohormone signals and secondary metabolism, providing foundations for crop improvement in combating barren ear tip.