Regulatory Control of Orchestrated Silk Elongation Moderated by Sugar Metabolism, Phytohormone Signaling, and Secondary Metabolite Dynamics

Background and Aims As the stigma of female flower in maize, silks emerge sequentially from ear base to apex, potentially causing barren ear tip. This study aimed 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 stages (T3), respectively. Key Results Silk extension rate and length progressively declined from ear base to apex, correlated with decreased hexose availability due to lower sucrose supply and weaker sucrose decomposition, as well as the gradient phytohormone deposition. Further comparative analyses on silk metabolomics and transcriptomics between three stages and three positions identified the stage-specific and position-specific genes and metabolites. The elongation of silks at three positions involves the 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 defense metabolism at T3. Position-specific pathways highlighted the earlier biosynthesis of secondary metabolites in basal silks, and delayed phytohormone signaling, starch and sucrose metabolism, and mitogen-activated protein kinase (MAPK) signaling in apical silks. At T3, silk senescence progressed from ear base to apex by having more severe sugar depletion, salicylic/jasmonic acids deposition, and active brassinosteroid/abscisic acid synthesis. Conclusions The sequential silk elongation on an ear is collectively coordinated by assimilates competition, phytohormone signals, and secondary metabolism, providing foundations for crop improvement in combating barren ear tip.