Prickle morphogenesis in rose is coupled with secondary metabolite accumulation and governed by canonical MBW transcriptional complex.

Unlabelled: Rose is an economically important flowering plant that holds an essential place in cut flower, medicinal, and aromatic industries. The presence of prickles, epidermal outgrowths resembling trichomes, on rose is highly undesirable as these make harvesting and transportation difficult. Attempts were made for generating rose varieties lacking prickles via breeding and natural selections; however, these approaches obtained only chimeric and genetically unstable prickle-less mutants. The alternative way to get rid of prickles is via genetic manipulations, but the molecular mechanisms of prickle initiation and development in rose are almost unexplored. Therefore, the present study was carried out to understand the morphological, molecular, and correlated metabolic changes underlining prickle morphogenesis in a prickle-bearing L. cv. "First Red (FR)". The histological and metabolomic analyses at three distinct stages of the prickle morphogenesis, namely, emerging tiny initiating prickles, partially greenish soft prickles, and brownish hard prickles, demonstrated a gradually increasing deposition of phenolic compounds and lignification with development. Corresponding RNAseq analysis revealed an upregulation of the genes involved in secondary metabolism, especially in the phenylpropanoid biosynthetic pathway. A set of genes encoding a transcriptional network similar to the one regulating epidermal cell differentiation leading to phenylpropanoid accumulation and trichome development, was also upregulated. Differential expression of this transcriptional network in prickle-less L. cv. "Himalayan Wonder" compared to prickly FR plants substantiated its involvement in prickle morphogenesis. The results collectively supported the proposition that prickles are evolved from trichomes and provided molecular clues towards engineering prickle-less roses.

Significance Statement: Prickles, the vasculature less epidermal outgrowths resembling trichomes, are defense organs protecting plants against herbivory. Despite biological significance, the mechanism of prickle morphogenesis remains obscure. Here, we show that like trichomes, prickles accumulate secondary metabolites, especially lignin and flavonoids, during morphogenesis. Cognate transcriptome analysis demonstrated that upregulation of a hormone-regulated transcriptional activation-inhibition network, known to govern trichome morphogenesis, likely triggers the differentiation of epidermal cells to outgrow into prickle.