Nonglandular prickle formation is associated with development and secondary metabolism‐related genes in Rosa multiflora

Abstract

Roses are among the most economically important ornamental plants worldwide. But prickles on the stem and leaves cause difficulties for cultivation or inconveniences during harvest and transportation, thus are an undesirable horticultural character. However, little is known about the molecular mechanisms of prickle development. In this study, we sought to develop Rosa multiflora (in the family Rosaceae) as a model plant to study prickle formation. The morphology, structure, and ontogeny of prickles were characterized, and transcriptome analysis of prickly and prickleless R. multiflora genotypes was performed. Morphological observation and microscopic analyses revealed that prickles of R. multiflora were non-glandular prickles (NGPs) and their maturation went through five developmental stages, which was accompanied by the accumulation of secondary metabolites such as lignin and anthocyanins. Comparative transcriptome analysis identified key pathways and hub genes potentially involved in prickle formation. Interestingly, among the differentially expressed genes (DEGs), several notable development and secondary metabolism-related transcription factors (TFs) including NAC, TCP, MYB, homeobox, and WRKY were up-regulated in prickly internodes. KEGG enrichment analysis indicated that DEGs were enriched in the pathways related to biosynthesis of secondary metabolites, flavonoids, and phenylpropanoids in the prickly R. multiflora. Our study provides novel insights into the molecular network underlying the regulation of prickle morphogenesis in R. multiflora, and the identified candidates might be applied to the genetic improvement of roses. | INTRODUCTIONSpinescence, including thorns, spines, and prickles, is a plant trait referring to the presence of sharp appendages with disparate origins, which bears ecological, evolutionary, and biogeographic significance. From a functional perspective, thorns, spines, and prickles are of analogous structures which have been evolved into a defense against herbivory (Givnish et al. 1994;Grubb 1992;Hanley et al. 2007). In addition, certain types of spinescence may represent effective adaptation to stresses, such as aridity, low temperatures, or extreme shortwave radiation (Nobel 2003). From a morphological perspective, thorns are modified twigs, branches, or stems, while spines are modified leaves, leaf parts, or stipules and prickles are simply outgrowths of epidermal and in some cases cortical tissues which lack of vasculature (Coyner et al. 2005;Posluszny & Fisher 2000). Prickles are widely distributed in many plants, and they can be found on the stems, branches, leaves, and fruits. Common plants with prickles are found in Rosaceae, such as Rosa chinensis, Rosa rugosa, Rosa multiflora, and Rubus idaeus, in Solanaceae such as Solanum viarum and Solanum rostratum, in Araliaceae such as A. spinosa and in Rutaceae such as Zanthoxylum bungeanum.

Comparative Transcriptome Analysis of Gleditsia sinensis Thorns at Different Stages of Development

“…PCA analysis showed that the three replicate samples in each same group could be clustered together well, indicating that the accuracy of this sequencing result was high. Several notable developments and secondary metabolism-related TFs including NAC , TCP , MYB , homeobox , and WRKY were up-regulated in prickly internodes of Rosa multiflora [ 13 ]. A large number of TFs could be involved in the formation and development of trichomes, and the accumulation of Rosa sterilis RsETC1 ( R3-MYB ) was significantly higher in inflorescence stems compared with pedicels [ 20 ].…”

“…The Lycium ruthenicum branch-thorns occur in response to drought and protect the corresponding axillary buds against drought stress [ 10 ]. Transcription factors such as MYB, bHLH, and TCP are involved in the development of prickles [ 11 , 12 , 13 ]. TCP TFs— THORN IDENTITY1 ( TI1 ) and TI2 , are expressed in axillary meristems and bind to the promoter of WUSCHEL, repressing the maintenance of cell proliferation [ 14 ].…”

Chromosome-levelde novogenome unveils the evolution ofGleditsia sinensisand thorns development

“…Genes expression profiling found that, PIN7 and LAX3 might be related with thorn phenotype of pummelo plant (Wu et al, 2021). Additionally, transcription factors such as TCP and NAC might regulate plant thorns development (Zhang et al, 2021; Zhang et al, 2021; Liu et al, 2023). With the increasing attention to the significant medicinal value of the Gleditsia , the molecular mechanism and gene regulation related to thorns development needs to be further elucidated.…”