The Muday Laboratory, Wake Forest University

Flavonoids as endogenous regulators of auxin transport

Polar transport of the plant hormone auxin controls many aspects of plant growth and development. A number of synthetic compounds have been shown to block the process of auxin transport by inhibition of the auxin efflux carrier complexes. These synthetic auxin transport inhibitors may act by mimicking endogenous molecules. Flavonoids, a class of secondary plant metabolic compounds, have been suggested to be endogenous auxin transport inhibitors based on their in vitro activity (Jacobs and Rubery, 1988). In collaboration with Dr.Angus Murphy and Dr. Wendy Peerflavonoids-light-and-dark (Purdue University), we have tested hypothesis that flavonoids regulate auxin transport in vivo in Arabidopsis thaliana by comparing wild-type and the tt4 mutant that does not synthesize flavonoids. Auxin transport is elevated in plants with a tt4 mutation (Brown et al. 2001). This elevated transport is reversed when flavonoid biosynthesis is restored by growth of plants on the flavonoid precursor, naringenin (Brown et al. 2001; Buer and Muday, 2004). Finally, the pattern of flavonoid accumulation in whole plants occurs in places appropriate for these compounds to control auxin transport related developmental phenotypes (Peer et al, 2001; Buer and Muday, 2004). Together our work in this area is consistent with a role for flavonoids as endogenous regulators of auxin transport.

Recent work has focused on understanding whether flavonoids regulate the response of roots to light and gravity. The tt4 mutation increases root basipetal IAA transport, consistent with the absence of a negative regulator of auxin transport (Buer and Muday, 2004) The initiation of gravitropic curvature in roots of multiple tt4 mutant alleles is reduced relative to wild-type and this inhibition is reversed by growth on naringenin (Buer and Muday, 2004; Buer et al., 2006). Gravitropic reorientation of wild-type roots induces flavonoid accumulation in the epidermal tissues of roots where basipetal IAA movement occurs. Together, these results indicate that flavonoids may act to modulate the movement of auxin to facilitate the early stages of root gravitropic bending (Buer and Muday, 2004). Additional experiments have provided evidence that enhanced flavonoid synthesis may be the mechanism by which ethylene reduces root gravitropic response. Not only are the levels of flavonoids enhanced in response to ethylene treatment, but the ability of ethylene to reduce root gravitropism is lost in the tt4 mutant that produces no flavonoids (Buer et al., 2006). Our current experiments are focused on understanding the molecular mechanisms for the cross talk between ethylene and auxin in control of root architecture and whether flavonoids have additional roles in this process.

Flavonoid biosynthesis is regulated by light. In dark grown seedlings, no flavonoid accumulation is detectable, but flavonoid accumulation is rapidly detectable in response to light (Buer and Muday, 2004), as shown in the associated image. This result suggests the hypothesis that mutants with altered light signaling may have phenotypes that are due to altered flavonoid synthesis that then alters auxin flow. We tested this possibility in collaboration with Dr. Christian Hardtke using the hy5 mutant, which has elongated hypocotyl phenotype in light grown seedlings and whose roots have delayed gravity response. We found that flavonoid synthesis was absent in light grown seedlings of hy5 and even though naringenin treatment restored wild-type levels of flavonoid synthesis, it did not restore root gravitropic response (Sibout et al. 2006). The presence of altered expression of auxin signaling genes suggests that the hy5 defect may be auxin dependent, but flavonoid independent.

(graduate students in bold, undergradutes underlined)

Lewis, DR, Ramirez, MV, Miller, ND, Keith, R, Helm, R, Winkel, BSJ, Muday, GK (In review) Auxin and ethylene induce distinct flavonol accumulation patterns through independent transcriptional networks: Plant Physiol

Buer, CS, Muday, GK, Djordjevic, MA (2008) Implications of long-distance flavonoid movement in Arabidopsis thaliana. Plant Signaling and Behavior: 3: 415-417

Buer, CS, Muday, GK, Djordjevic, MA (2007) Flavonoids are transported long distances in Arabidopsis. Plant Physiol. 145: 478-490.

Buer, CS, and Muday, GK (2004) The transparent testa4 mutation prevents flavonoid synthesis and alters auxin transport and the response of Arabidopsis roots to gravity and light. Plant Cell, 16: 1191-1205.

Buer, CS, Sukumar, P, and Muday, GK (2006) Ethylene induced flavonoid synthesis modulates root gravitropism. Plant Physiology: 140: 1384-1396

Brown, DE, Rashotte, AM, Murphy, AS, Normanly, J, Tague, BW, Peer , WS, Taiz ,L , and Muday, GK (2001) Flavonoids act as negative regulators of auxin transport in vivo in Arabidopsis. Plant Physiol 126: 524-535

Jacobs M, Rubery PH (1988) Naturally occurring auxin transport regulators. Science 241: 346-349

Peer, WA, Murphy, AS, Brown, DE, Tague, BW, Muday, GK, Taiz, L.(2001) Flavonoid accumulation patterns in transparent testa mutants of Arabidopsis. Plant Physiol. 126: 536-548

see also [Pubmed List of Papers]


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