UVR8‐mediated induction of flavonoid biosynthesis for UVB tolerance is conserved between the liverwort Marchantia polymorpha and flowering plants

Abstract

Damaging UVB radiation is a major abiotic stress facing land plants. In angiosperms the UV RESISTANCE LOCUS8 (UVR8) photoreceptor coordinates UVB responses, including inducing biosynthesis of protective flavonoids. We characterised the UVB responses of Marchantia polymorpha (marchantia), the model species for the liverwort group of basal plants. Physiological, chemical and transcriptomic analyses were conducted on wild-type marchantia exposed to three different UVB regimes. CRISPR/Cas9 was used to obtain plant lines with mutations for components of the UVB signal pathway or the flavonoid biosynthetic pathway, and transgenics overexpressing the marchantia UVR8 sequence were generated. The mutant and transgenic lines were analysed for changes in flavonoid content, their response to UVB exposure, and transcript abundance of a set of 48 genes that included components of the UVB response pathway characterised for angiosperms. The marchantia UVB response included many components in common with Arabidopsis, including production of UVB-absorbing flavonoids, the central activator role of ELONGATED HYPOCOTYL5 (HY5), and negative feedback regulation by REPRESSOR OF UV-B PHOTOMORPHOGENESIS1 (RUP1). Notable differences included the greater importance of CHALCONE ISOMERASE-LIKE (CHIL). Mutants disrupted in the response pathway (hy5) or flavonoid production (chalcone isomerase, chil) were more easily damaged by UVB. Mutants (rup1) or transgenics (35S:MpMYB14) with increased flavonoid content had increased UVB tolerance. The results suggest that UVR8-mediated flavonoid induction is a UVB tolerance character conserved across land plants and may have been an early adaptation to life on land.

Rice sulfoquinovosyltransferase SQD2.1 mediates flavonoid glycosylation and enhances tolerance to osmotic stress

“…One significant feature of flavonoids is their high ROS-scavenging capacity, which is attributed to their ability to protect cells from oxidative damage under UV light, fungal infection, and insect herbivory (Clayton et al, 2018;Heim, Tagliaferro, & Bobilya, 2002;Stracke, Favory, et al, 2010;Zhang et al, 2013;Zhang et al, 2015). Defective flavonoid accumulation resulted in enhanced H 2 O 2 in plant tissues (Nakabayashi et al, 2014).…”

“…A series of flavonoid subclasses, including flavonols, flavones, proanthocyanidins, and anthocyanins, have been identified in plants and function as antioxidants to protect against oxidative stress and cell damage (Clayton et al, 2018;Dixon & Paiva, 1995;Do & Cormier, 1990;Vickers, Gershenzon, Lerdau, & Loreto, 2009). Flavonoids are widely distributed in different cell compartments, including the cytosol, endoplasmic reticulum, vacuole, chloroplast, nucleus, small vesicles, and extracellular space (Agati, Matteini, Goti, & Tattini, 2007;Petrussa et al, 2013;Saslowsky, Warek, & Winkel, 2005;Saunders & McClure, 1976;Xu et al, 2015;Zhao & Dixon, 2010).…”

Auronidins are a previously unreported class of flavonoid pigments that challenges when anthocyanin biosynthesis evolved in plants

“…However, although more than 8,000 individual flavonoid structures have been characterized (6), the great majority belong to a small number of major flavonoid classes. All land plants studied to date, including the liverworts, considered the probable basal plant group, produce nearly colorless, vacuolar-located flavone or flavonol glycosides, which absorb UV light and are important for ameliorating the damaging effects of UV-B radiation (1,(7)(8)(9)(10)(11)(12). Seed plants also produce a variety of vacuolarlocated anthocyanidin glycosides (anthocyanins) (13) that provide the majority of water-soluble plant colors, ranging from orange to blue.…”

“…Anthocyanins share the same initial biosynthetic steps as flavones/flavonols but require additional enzymatic steps that are well defined in seed plants but not in nonseed plants. It is assumed that the branches of the flavonoid biosynthetic pathway that lead to flavones/flavonols and anthocyanins arose during the evolutionary transition of plants from aquatic to land environments (1,3,(7)(8)(9).…”

Genome-wide analysis of MpBHLH12, a IIIf basic helix-loop-helix transcription factor of Marchantia polymorpha

“…Mapoly0047s0001 was the only gene significantly down-regulated in MpBHLH12ox lines; however, this gene was significantly up-regulated in MpMYB14 ectopic expression lines. According to a recent publication by Clayton et al (2018), UVB irradiation induces flavonoids and does not induce MpBHLH12 expression. Moreover, the expression of chalcone isomerase and chalcone isomeraselike genes induced by UVB is not affected in MpBHLH12ox lines, suggesting that the GRN of MpBHLH12 is distinct from that of flavonoid biosynthesis genes regulated by MpMYB14.…”