Contrastive analysis of trichome distribution, morphology, structure, and associated gene expression reveals the formation factors of different trichome types in two commercial Rosa species

Abstract

Trichomes are prevalent on the surfaces of many organs in Rosa and have an important impact on the edibility of the fruit. Here, the diversity, distribution, anatomical structure, and genetic regulation of trichomes in Rosa roxburghii Tratt. (RR) and R. sterilis S. D. Shi (RS) were explored. RS and RR are important commercial crops in China due to their nutritional and medicinal value; however, their consumption and utilization are limited, in part, by the abundance of trichomes on the fruit. Two main forms of trichomes were present in both germplasms, namely glandular and non-glandular trichomes. Non-glandular flagellate and acicular trichomes were observed on the sepals, fruit, major leaf veins, and pedicels of both germplasms, whereas non-glandular branched trichomes were present only on RS. Flagellate trichome exfoliation and acicular trichome lignification occurred gradually on the developing fruit. Capitate glandular and bowl-shaped glandular trichomes were abundant in RS, but were only observed on the major leaf veins of RR. Furthermore, some capitate glandular trichomes on the pedicels were found to develop into prickles in RS. Transmission electron microscopy indicated that vacuolation and in the extraplasmic space occurred in the glandular cells of the capitate trichomes at the late secretory stage. The prickles in RR and RS mainly consisted of lignin, suberin, cellulose, and hemicellulose, though the ratios of these constituents varied between species. The expression levels of several well-known core trichome regulatory genes varied depending on the trichome type. The transcript abundance of GL1, GL2, and TTG1 was significantly higher in organs covered with acicular trichomes in both RR and RS, while the highest mRNA level of TRY was observed in the glabrous organs, suggesting a negative effect of this gene on trichome formation. Notably, the negative regulatory factor CPC was only highly expressed in the leaf mesophyll of RR, where no glandular trichomes were present, and the GL3, PDF2-like, and CPC transcription factors co-regulated glandular trichome formation in RS. The expression of these genes peaked in the Fb3-stage buds of RR and B3-stage buds of RS, indicating different key phases for the regulation of trichome initiation. These data provide new insights into the genetic control of trichome formation in two Rosa species.