The anthocyanin reduced Tomato Mutant Demonstrates the Role of Flavonols in Tomato Lateral Root and Root Hair Development

Abstract

This study utilized tomato (Solanum lycopersicum) mutants with altered flavonoid biosynthesis to understand the impact of these metabolites on root development. The mutant anthocyanin reduced (are) has a mutation in the gene encoding FLAVONOID 3-HYDROXYLASE (F3H), the first step in flavonol synthesis, and accumulates higher concentrations of the F3H substrate, naringenin, and lower levels of the downstream products kaempferol, quercetin, myricetin, and anthocyanins, than the wild type. Complementation of are with the p35S:F3H transgene reduced naringenin and increased flavonols to wild-type levels. The initiation of lateral roots is reduced in are, and p35S:F3H complementation restores wild-type root formation. The flavonoid mutant anthocyanin without has a defect in the gene encoding DIHYDROFLAVONOL REDUCTASE, resulting in elevated flavonols and the absence of anthocyanins and displays increased lateral root formation. These results are consistent with a positive role of flavonols in lateral root formation. The are mutant has increased indole-3-acetic acid transport and greater sensitivity to the inhibitory effect of the auxin transport inhibitor naphthylphthalamic acid on lateral root formation. Expression of the auxin-induced reporter (DR5-b-glucuronidase) is reduced in initiating lateral roots and increased in primary root tips of are. Levels of reactive oxygen species are elevated in are root epidermal tissues and root hairs, and are forms more root hairs, consistent with a role of flavonols as antioxidants that modulate root hair formation. Together, these experiments identify positive roles of flavonols in the formation of lateral roots and negative roles in the formation of root hairs through the modulation of auxin transport and reactive oxygen species, respectively.

Flavonols Mediate Root Phototropism and Growth through Regulation of Proliferation-to-Differentiation Transition

“…Based on our model (Figure 10), differential accumulation of flavonols on the illuminated side of the root, which likely requires cytokinin signaling, may affect the transport of auxin, causing its asymmetric distribution and signaling. Flavonols also acts as ROS scavengers in Arabidopsis and tomato plants (Maloney et al, 2014;Watkins et al, 2014). ROS generation and signaling are involved in root tropic responses (Joo et al, 2001;Clore et al, 2008).…”

“…In this regard, we show that a low concentration of auxin can trigger O 2 2 production that might promote cell division in dark-grown roots. However, this auxin-O 2 2 mechanism might be counteracted by the ROS-scavenger potential of flavonols (Maloney et al, 2014;Watkins et al, 2014). An additional aspect of the flavonol-dependent connection between auxin-cytokinin and ROS pathways is that as cytokinin and H 2 O 2 regulate the accumulation of flavonols in darkness, both can restrict O 2 2 levels and affect auxin transport, creating a complex regulatory mechanism.…”

“…NADPH participates in the production of O 2 2 (Foreman et al, 2003). O 2 2 promotes cell proliferation (Dunand et al, 2007;Tsukagoshi et al, 2010), while flavonols may function as ROS scavengers (Pietta, 2000;Maloney et al, 2014;Watkins et al, 2014). Thus, we decided to analyze the interaction of O 2 2 and flavonol accumulation in the regulation of the root meristem size.…”

“…Flavonols inhibit auxin transport, as shown by genetic analyses of mutants that do not synthesize them or by exogenous treatment of wild-type plants with flavonols Peer et al, 2001Peer et al, , 2004Peer and Murphy, 2014). Moreover, flavonols can act as in vivo reactive oxygen species (ROS) scavengers in Arabidopsis thaliana and in tomato (Solanum lycopersicum) plants (Maloney et al, 2014;Watkins et al, 2014) and interfere with indole-3-acetic acid (IAA) catabolism (Peer et al, 2004(Peer et al, , 2013. Previous studies have shown that in vitro-grown roots, which are routinely exposed to illumination, accumulate high levels of flavonols (Buer and Muday, 2004).…”

Focus on Roots

“…The article by Maloney et al (2014) reports on the effect of flavonols on auxin transport and lateral root formation. The articles by Saengwilai et al (2014) and Postma et al (2014) highlight how root system architecture can influence the capacity of roots toward efficient nitrate uptake and how different architectures are optimal for uptake of distinct nutrients.…”