The Role of Anthocyanins in Plant Tolerance to Drought and Salt Stresses

Abstract

Drought and salinity affect various biochemical and physiological processes in plants, inhibit plant growth, and significantly reduce productivity. The anthocyanin biosynthesis system represents one of the plant stress-tolerance mechanisms, activated by surplus reactive oxygen species. Anthocyanins act as ROS scavengers, protecting plants from oxidative damage and enhancing their sustainability. In this review, we focus on molecular and biochemical mechanisms underlying the role of anthocyanins in acquired tolerance to drought and salt stresses. Also, we discuss the role of abscisic acid and the abscisic-acid-miRNA156 regulatory node in the regulation of drought-induced anthocyanin production. Additionally, we summarise the available knowledge on transcription factors involved in anthocyanin biosynthesis and development of salt and drought tolerance. Finally, we discuss recent progress in the application of modern gene manipulation technologies in the development of anthocyanin-enriched plants with enhanced tolerance to drought and salt stresses.

Keywords: abiotic stress; abscisic acid; anthocyanin; drought; microRNA; salinity stress; transcription factors (TFs).

Figure 1

Schematic representation of the anthocyanin biosynthesis pathway. Genes in magenta boxes: PAL (phenylalanine ammonia-lyase); C4H (cinnamate-4-hydroxylase); 4CL (4-coumarate-CoA ligase); CHS (chalcone synthase); CHI (chalcone isomerase); FNS (flavone synthase); F3H (flavanone 3-hydroxylase); F3′H (flavonoid 3′-hydroxylase); F3′5′H (flavonoid 3′,5′-hydroxylase); FLS (flavonol synthase); DFR (dihydroflavonol 4-reductase); LAR (leucoanthocyanidin reductase); LDOX (leucoanthocyanidin dioxygenase); OMT (O-methyltransferase); ANS (leucoanthocyanidin dioxygenase); ANR (anthocyanidin reductase); UFGT (UDP-glucose: flavonoid 3-O-glucosyltransferase); and GST (glutathione S-transferase).

Figure 2

Schematic representation of miR156-ABA-based regulatory module of drought tolerance and induction of anthocyanin biosynthesis. Under drought conditions, the increased ABA level reduced stomatal aperture and promoted anthocyanin biosynthesis, thus increasing anthocyanin concentrations. Furthermore, acting via the Ca²⁺ sensor CPK, drought induced miR156, which, in turn, silenced SPLs and increased levels of WD40-1, thus enhancing anthocyanin accumulation. Arrows represent activation; blunt arrows—repression; dashed arrow—the involvement of several intermedium steps; and magenta arrows—increased levels of corresponding metabolites. Blue box—ABA (abscisic acid); green box—ABA-R (abscisic acid receptor); yellow oval—CPK (Ca²⁺-dependent protein kinase); ROS (reactive oxygen species); and SPL (squamosa promoter binding protein-like) gene.

Figure 3

A model of TFs regulating anthocyanin biosynthesis and tolerance to drought. Drought-regulated anthocyanin production and the development of drought stress tolerance through the set of TFs—positive and negative regulators. Some TFs (such as NAC019 and CBF3) can be defined as “master regulators” because they also orchestrate the expression of other TFs regulating anthocyanin biosynthesis. NAC019 acted as a purely negative regulator of stress-induced anthocyanin biosynthesis and drought tolerance, while CBF3 negatively regulated all processes except “drought tolerance”. Magenta boxes depict TFs discussed in this section; yellow boxes—TFs known to regulate anthocyanin biosynthesis. The “Osmoprotectors” box represents proline, soluble sugars, and carbohydrates; “Antioxidants”—CAT (catalase), POD (peroxidase), SOD (superoxide dismutase), and glutathione. Arrows represent positive regulation and blunt thick lines—negative regulation. NAC (No Apical Meristem/NAM, Arabidopsis ATAF1/2, and Cup-shaped Cotyledon2/CUC2); CBF (C-repeat-binding factor); GL3 (GLABRA 3); MYB (myeloblastosis); TTG1 (TRANSPARENT TESTA GLABRA 1); PAP1 (PRODUCTION OF ANTHOCYANIN PIGMENT); ERF (ethylene response factor); C3H35 (ZINC FINGER CCCH DOMAIN-CONTAINING PROTEIN 35); and Lc (leaf colour). Taxonomic affiliation: Bo (Brassica oleracea L); Lr (Lycoris radiata (L’Hér.) Herb); Vy (Vitis yanshanesis J. X. Chen.); Ct (Carthamus tinctorius L.); Md (Malus × domestic); Pu (Populus ussuriensis Kom.); Sc (Chaenomeles speciosa (Sweet) Nak.); Zm (Zea mays L.); and TFs with no affiliation belong to Arabidopsis thaliana (L.) Heynh.

Figure 4

A model of TFs regulating anthocyanin biosynthesis and tolerance to salt stress. Salt stress-regulated anthocyanin biosynthesis and the development of tolerance to salt stress through the set of TFs—positive and negative regulators. DRB3 and MdZAT5 acted oppositely as a negative regulator of anthocyanin biosynthesis and a positive regulator of salt stress tolerance (for DRB3) and vice versa (for MdZAT5), respectively. MYB3 and ANAC032 acted as negative and MYB112 as positive master regulators because they regulated a set of other TFs regulating anthocyanin biosynthesis. Magenta boxes depict TFs discussed in this section; yellow boxes—TFs known to regulate anthocyanin biosynthesis. “Antioxidants”—CAT (catalase), POD (peroxidase), SOD (superoxide dismutase), and glutathione. Arrows represent positive regulation and blunt thick lines—negative regulation. GL3 (GLABRA 3); MYB (myeloblastosis); TTG1 (TRANSPARENT TESTA GLABRA 1); PAP1 (PRODUCTION OF ANTHOCYANIN PIGMENT); PL1/C1 (PURPLE PLANT1/COLORED ALEURONE1); ZAT (zinc finger of Arabidopsis thaliana); and DRB (double-stranded RNA-binding protein).

Figure 5

The role of anthocyanins in the development of abiotic-stress-tolerant plants. Abiotic stresses negatively affect plants and cause different physiological, biochemical, and molecular responses through activation of various transcription factors. Together with other adaptive mechanisms (such as osmolyte and antioxidant production, and increased ABA biosynthesis), increased anthocyanin biosynthesis and accumulation is aimed to reshape plant physiological, metabolic, and morphological parameters in order to make them more tolerant to various abiotic stresses and to improve their productivity.