Flavonoid deficiency disrupts redox homeostasis and terpenoid biosynthesis in glandular trichomes of tomato

Abstract

Glandular trichomes are epidermal structures that provide a first line of chemical defense against arthropod herbivores and other biotic threats. The most conspicuous structure on leaves of cultivated tomato (Solanum lycopersicum) is the type-VI glandular trichome (tVI-GT), which accumulates both flavonoids and volatile terpenoids. Although these classes of specialized metabolites are derived from distinct metabolic pathways, previous studies with a chalcone isomerase 1 (CHI1)-deficient mutant called anthocyanin free (af) showed that flavonoids are required for terpenoid accumulation in tVI-GTs. Here, we combined global transcriptomic and proteomic analyses of isolated trichomes as a starting point to show that the lack of CHI1 is associated with reduced levels of terpenoid biosynthetic transcripts and enzymes. The flavonoid deficiency in af trichomes also resulted in the upregulation of abiotic stress-responsive genes associated with DNA damage and repair. Several lines of biochemical and genetic evidence indicate that the terpenoid defect in af mutants is specific for the tVI-GT and is associated with the absence of bulk flavonoids rather than loss of CHI1 per se. A newly developed genome-scale model of metabolism in tomato tVI-GTs helped identify metabolic imbalances caused by the loss of flavonoid production. We provide evidence that flavonoid deficiency in this cell type leads to increased production of reactive oxygen species (ROS), which may impair terpenoid biosynthesis. Collectively, our findings support a role for flavonoids as ROS-scavenging antioxidants in glandular trichomes.

Mutations that alter Arabidopsis flavonoid metabolism affect the circadian clock

“…Flavonoid bioactivity has invariably been ascribed to the strong antioxidant potential of these compounds, which can be present at quite high levels in certain tissues and in response to diverse biotic and abiotic stresses, although this remains a matter of substantial debate (Agati et al., 2020). There is good evidence that flavonoids do function as antioxidants in some situations, for example, in glandular trichomes, where lack of flavonoids increases production of ROS (Sugimoto et al., 2021), and in protecting plant tissues from oxidative stress associated with drought or high temperatures (Muhlemann et al., 2018; Nakabayashi et al., 2014). There is also a strong connection between the clock and the intracellular redox state in plants, which is modulated both by endogenous metabolic processes, including respiration and photosynthesis, and by environmental conditions that elevate intracellular ROS (Guadagno et al., 2018).…”

Natural variation in the transcription factor REPLUMLESS contributes to both disease resistance and plant growth in Arabidopsis

“…Future studies should assess whether these mutants recover the growth defect of the rpl mutants. Furthermore, transcriptomic and proteomic analyses of a chi mutant in tomato showed that flavonoid deficiency probably impairs terpenoid biosynthesis, which is important for preventing biotic threats such as arthropod herbivores ( Sugimoto et al., 2022 ). Therefore, RPL-directed CHI expression may be involved in both plant defense and growth in tomato.…”

Identification and characterization of a novel gene involved in glandular trichome development in Nepeta tenuifolia

“…In addition to the cuticle and trichome, the impact of flavonoid and terpenoid biosynthetic pathways, and trichome development was recently demonstrated in tomato and A. annua (Kang et al, 2014;Shi et al, 2018;Sugimoto et al, 2021). The af mutated tomato, AaYABBY5-overexpressed, and AaTAR2overexpressed A. annua all affect trichome density, flavonoid, and terpenoid biosynthesis (Kayani et al, 2019(Kayani et al, , 2021Zhou et al, 2020;Sugimoto et al, 2021).…”

“…In addition to the cuticle and trichome, the impact of flavonoid and terpenoid biosynthetic pathways, and trichome development was recently demonstrated in tomato and A. annua (Kang et al, 2014;Shi et al, 2018;Sugimoto et al, 2021). The af mutated tomato, AaYABBY5-overexpressed, and AaTAR2overexpressed A. annua all affect trichome density, flavonoid, and terpenoid biosynthesis (Kayani et al, 2019(Kayani et al, , 2021Zhou et al, 2020;Sugimoto et al, 2021). Our findings demonstrated that terpenoid-related genes and terpenoid metabolites were downregulated in plants with fewer PGTs, compared to controls; however, the variation in flavonoid contents in control plants and plants with fewer PGTs was not significant.…”

“…GT initiation is also implicated in cuticle biosynthesis; however, the relationship between trichome formation and cutin and wax biosynthesis remains unknown. Intriguingly, in addition to terpenoids, GT initiation also affects flavonoid biosynthesis, even though these two pathways operate independently (Sugimoto et al, 2021). The tomato mutant odorless-2 (od-2) exhibits defects in the development and density of GTs, as well as a disruption in the production of terpenes and flavonoids (Kang et al, 2010).…”