Loss of type-IV glandular trichomes is a heterochronic trait in tomato and can be reverted by promoting juvenility

Abstract

Glandular trichomes are structures with widespread distribution and deep ecological significance. In the Solanum genus, type-IV glandular trichomes provide resistance to insect pests. The occurrence of these structures is, however, poorly described and controversial in cultivated tomato (Solanum lycopersicum). Optical and scanning electron microscopy were used to screen a series of well-known commercial tomato cultivars, revealing the presence of type-IV trichomes on embryonic (cotyledons) and juvenile leaves. A tomato line overexpressing the microRNA miR156, known to promote heterochronic development, and mutants affecting KNOX and CLAVATA3 genes possessed type-IV trichomes in adult leaves. A re-analysis of the Woolly (Wo) mutant, previously described as enhancing glandular trichome density, showed that this effect only occurs at the juvenile phase of vegetative development. Our results suggest the existence of at least two levels of regulation of multicellular trichome formation in tomato: one enhancing different types of trichomes, such as that controlled by the WOOLLY gene, and another dependent on developmental stage, which is fundamental for type-IV trichome formation. Their combined manipulation could represent an avenue for biotechnological engineering of trichome development in plants.

The ratio of trichomes to stomata is associated with water use efficiency in Solanum lycopersicum (tomato)

“…These differences were likely to have resulted from differences in the age of the plant as well as changes in environmental conditions between the glasshouse and the field. Trichome development is reported to change with the age of the plant (Telfer et al ., ; Vendemiatti et al ., ), with higher TD observed in the late leaves of tomato (Gurr and McGrath, ). Moreover, environmental factors, such as temperature, photoperiod, light intensity or soil humidity have direct effects on trichome development in several species, including tomato (Wellso and Hoxie, ; Gianfagna et al ., ; Chien and Sussex, ; Souza et al ., ).…”

“…These differences were likely to have resulted from differences in the age of the plant as well as changes in environmental conditions between the glasshouse and the field. Trichome development is reported to change with the age of the plant (Telfer et al, 1997;Vendemiatti et al, 2017), with higher TD observed in the late leaves of tomato (Gurr and McGrath, 2001).…”

Genetic factors outside the metabolic cluster for plastid-derived sesquiterpenes are required to pursue arthropod-resistant tomatoes

“…Furthermore, MT- Sst2 displayed an increased number of type-V non-glandular trichomes compared to both MT and LA1777 (Fig 5B). It was shown earlier that there appears to be a negative correlation between densities of glandular type-IV trichomes and the non-glandular type-V trichomes (Vendemiatti et al , 2017). The lower density of type-V trichomes in LA1777 could therefore be related to its high density of type-IV trichomes.…”

“…5B). This lack of type-IV trichomes in cultivated tomato has been linked to the transition from the juvenility to the adult phase (Vendemiatti et al , 2017). So, the region introgressed in MT- Sst2 is most likely not involved in heterochrony and/or type-IV trichome development, though we cannot discard the possibility that the region introgressed harbors genes controlling the density of type-V trichomes, as we cannot explain the increased type-V density in the introgression line compared to MT.…”

“…Counting of trichomes density (mm 2 ) were performed on leaflets taken from mature fifth leaves (counting from cotyledons) according to the methodology described by Vendemiatti et al (2017). Both leaf surfaces were dissected along the longitudinal axis in 15 × 3 mm strips covering the middle section of the leaf blade (avoiding the primary veins).…”