Promoter replacement of ANT1 induces anthocyanin accumulation and triggers the shade avoidance response through developmental, physiological and metabolic reprogramming in tomato

Abstract

The accumulation of anthocyanins is a well-known response to abiotic stresses in many plant species. However, knowledge about the effects of excessive anthocyanin accumulation on light absorbance and photosynthesis is limited. Here, we addressed this question using a promoter replacement line of tomato constitutively expressing a MYB transcription factor (ANTHOCYANIN1, ANT1) that leads to anthocyanin accumulation. The genetic engineered ANT1 plants displayed traits associated with shade avoidance response: thinner leaves, lower seed germination rate, suppressed side branching, increased chlorophyll concentration, and lower photosynthesis rates than the wild type. Moreover, anthocyanin-rich leaves exhibited higher absorbance of light in the blue and red ends of the spectrum, while the increase in leaf energy dissipation and higher anthocyanin content in leaves provided photoprotection to high irradiance. Furthermore, analysis of key genes expression and primary metabolites content showed that anthocyanin accumulation produces a reconfiguration of both networks that is consistent, but not identical to the one described for the shade avoidance response. Our study provides clues about how anthocyanins accumulation affects the trade-off between photoprotection and growth.

SlAN1 is a limiting factor for the light-dependent anthocyanin accumulation in fruit tissues of purple tomato

“…Anthocyanin accumulation is commonly restricted to the subepidermal cells and absent in the parenchymal cells of the mesocarp, mesophyll, and cortex. Substrate is likely to be available in these cells since the expression of specific transgenic MYB and bHLH transcription factors leads to high anthocyanin accumulation in the inner tissues of the tomato fruit (Butelli et al ., 2008; Cerqueira et al ., 2023). Therefore, other mechanisms should explain this “parenchymal recalcitrance”, a widespread phenomenon throughout the angiosperms (Chaves-Silva et al ., 2018).…”

“…Beyond the ecological notion that anthocyanins are responsible for attracting pollinators and seed dispersers, they also play a protective role due to their antioxidant activity by scavenging reactive oxygen species (ROS) that otherwise could severely damage plant tissues (Buer et al ., 2010; Corso et al ., 2020). Furthermore, it has been suggested that anthocyanins form a protective barrier in plant tissues by absorbing the UV-B radiation potentially harmful to the photosynthetic machinery (Gould et al ., 2010; Cerqueira et al ., 2023). These properties make anthocyanins an important protective compound against environmental stresses.…”