Flavonoids Redirect PIN-mediated Polar Auxin Fluxes during Root Gravitropic Responses

The rate, polarity, and symmetry of the flow of the plant hormone auxin are determined by the polar cellular localization of PIN-FORMED (PIN) auxin efflux carriers. Flavonoids, a class of secondary plant metabolites, have been suspected to modulate auxin transport and tropic responses. Nevertheless, the identity of specific flavonoid compounds involved and their molecular function and targets in vivo are essentially unknown. Here we show that the root elongation zone of agravitropic pin2/eir1/wav6/agr1 has an altered pattern and amount of flavonol glycosides. Application of nanomolar concentrations of flavonols to pin2 roots is sufficient to partially restore root gravitropism. By employing a quantitative cell biological approach, we demonstrate that flavonoids partially restore the formation of lateral auxin gradients in the absence of PIN2. Chemical complementation by flavonoids correlates with an asymmetric distribution of the PIN1 protein. pin2 complementation probably does not result from inhibition of auxin efflux, as supply of the auxin transport inhibitor N-1-naphthylphthalamic acid failed to restore pin2 gravitropism. We propose that flavonoids promote asymmetric PIN shifts during gravity stimulation, thus redirecting basipetal auxin streams necessary for root bending. The rate, polarity, and symmetry of the flow of the plant hormone auxin are determined by the polar cellular localization of PIN-FORMED (PIN) auxin efflux carriers. Flavonoids, a class of secondary plant metabolites, have been suspected to modulate auxin transport and tropic responses. Nevertheless, the identity of specific flavonoid compounds involved and their molecular function and targets in vivo are essentially unknown. Here we show that the root elongation zone of agravitropic pin2/eir1/wav6/agr1 has an altered pattern and amount of flavonol glycosides. Application of nanomolar concentrations of flavonols to pin2 roots is sufficient to partially restore root gravitropism. By employing a quantitative cell biological approach, we demonstrate that flavonoids partially restore the formation of lateral auxin gradients in the absence of PIN2. Chemical complementation by flavonoids correlates with an asymmetric distribution of the PIN1 protein. pin2 complementation probably does not result from inhibition of auxin efflux, as supply of the auxin transport inhibitor N-1-naphthylphthalamic acid failed to restore pin2 gravitropism. We propose that flavonoids promote asymmetric PIN shifts during gravity stimulation, thus redirecting basipetal auxin streams necessary for root bending. The plant hormone auxin (3-indolyl acetic acid, IAA) 5The abbreviations used are: IAA, 3-indolyl acetic acid; PAT, polar auxin transport; NPA, N-1-naphthylphthalamic acid; EZ, elongation zone; RT, root tip; HPLC, high performance liquid chromatography; DPBA, diphenylboric acid 2-aminoethyl ester; MS, mass spectrometry; GFP, green fluorescent protein. 5The abbreviations used are: IAA, 3-indolyl acetic acid; PAT, polar auxin transport; NPA, N-1-naphthylphthalamic acid; EZ, elongation zone; RT, root tip; HPLC, high performance liquid chromatography; DPBA, diphenylboric acid 2-aminoethyl ester; MS, mass spectrometry; GFP, green fluorescent protein. controls virtually all plant developmental and physiological processes. In roots, the differential growth response associated with gravity stimulation (gravitropism) occurs in the elongation zone (1Muday G.K. J. Plant Growth Regul. 2001; 20: 226-243Crossref PubMed Scopus (144) Google Scholar, 2Chen R. Hilson P. Sedbrook J. Rosen E. Caspar T. Masson P.H. Proc. Natl. Acad. Sci. U. S. A. 1998; 95: 15112-15117Crossref PubMed Scopus (367) Google Scholar) and is a result of the asymmetric distribution of auxin to the lower side of epidermal cells (3Moore I. Curr. Biol. 2002; 12: R452-R454Abstract Full Text Full Text PDF PubMed Scopus (41) Google Scholar). In these tissues accumulating auxin, cell elongation is inhibited and the root tip bends downwards. This cell-to-cell or polar auxin transport (PAT) is determined by the asymmetric cellular localization of auxin in- and efflux components of the ABCB/PGP/MDR, AUX1/LAX, and PIN-FORMED (PIN) family (4Vieten A. Sauer M. Brewer P.B. Friml J. Trends Plant Sci. 2007; 12: 160-168Abstract Full Text Full Text PDF PubMed Scopus (257) Google Scholar, 5Wisniewska J. Xu J. Seifertova D. Brewer P.B. Ruzicka K. Blilou I. Rouquie D. Benkova E. Scheres B. Friml J. Science. 2006; 312: 883Crossref PubMed Scopus (662) Google Scholar, 6Geisler M. Murphy A.S. FEBS Lett. 2006; 580: 1094-1102Crossref PubMed Scopus (293) Google Scholar, 7Kerr I.D. Bennett M.J. Biochem. J. 2007; 401: 613-622Crossref PubMed Scopus (63) Google Scholar). Although ABCBs are apparently involved in long-range auxin transport and movements of auxin out of apical regions (8Blakeslee J.J. Bandyopadhyay A. Lee O.R. Mravec J. Titapiwatanakun B. Sauer M. Makam S.N. Cheng Y. Bouchard R. Adamec J. Geisler M. Nagashima A. Sakai T. Martinoia E. Friml J. Peer W.A. Murphy A.S. Plant Cell. 2007; 19: 131-147Crossref PubMed Scopus (326) Google Scholar, 9Lewis D.R. Miller N.D. Splitt B.L. Wu G. Spalding E.P. Plant Cell. 2007; 19: 1838-1850Crossref PubMed Scopus (151) Google Scholar, 10Wu G. Lewis D.R. Spalding E.P. Plant Cell. 2007; 19: 1826-1837Crossref PubMed Scopus (129) Google Scholar), AUX1 and PIN2/EIR1/WAV6AGR1 have been demonstrated to channel auxin from the lateral root cap basipetally to the expanding epidermal cells (11Swarup R. Friml J. Marchant A. Ljung K. Sandberg G. Palme K. Bennett M. Genes Dev. 2001; 15: 2648-2653Crossref PubMed Scopus (469) Google Scholar, 12Marchant A. Kargul J. May S.T. Muller P. Delbarre A. Perrot-Rechenmann C. Bennett M.J. EMBO J. 1999; 18: 2066-2073Crossref PubMed Scopus (454) Google Scholar, 13Abas L. Benjamins R. Malenica N. Paciorek T. Wisniewska J. Moulinier-Anzola J.C. Sieberer T. Friml J. Luschnig C. Nat. Cell Biol. 2006; 8: 249-256Crossref PubMed Scopus (455) Google Scholar). The regulation of auxin transport during root gravitropic responses is still largely unclear. Among various possible mechanisms, the localized synthesis and directed transport of flavonoids, plant-specific phenylpropanoid compounds, have been shown to modulate the rate of the gravity response (14Buer C.S. Muday G.K. Plant Cell. 2004; 16: 1191-1205Crossref PubMed Scopus (312) Google Scholar, 15Buer C.S. Muday G.K. Djordjevic M.A. Plant Physiol. 2007; 145: 478-490Crossref PubMed Scopus (192) Google Scholar). A number of lines of experimentation have suggested that flavonoids may act as non-essential auxin transport inhibitors (16Brown D.E. Rashotte A.M. Murphy A.S. Normanly J. Tague B.W. Peer W.A. Taiz L. Muday G.K. Plant Physiol. 2001; 126: 524-535Crossref PubMed Scopus (555) Google Scholar, 17Murphy A. Peer W.A. Taiz L. Planta. 2000; 211: 315-324Crossref PubMed Scopus (282) Google Scholar, 18Peer W.A. Bandyopadhyay A. Blakeslee J.J. Makam S.I. Chen R.J. Masson P.H. Murphy A.S. Plant Cell. 2004; 16: 1898-1911Crossref PubMed Scopus (305) Google Scholar, 19Peer W.A. Murphy A.S. Grotewold E. The Science of Flavonoids. Springer, Berlin2006: Scopus Google Scholar, W.A. Murphy A.S. Trends Plant Sci. 2007; 12: Full Text Full Text PDF PubMed Scopus Google Scholar). This is the that flavonoids of auxin transport N-1-naphthylphthalamic acid a in M. P.H. Science. PubMed Scopus Google Scholar, Plant Growth Regul. 2000; PubMed Scopus Google Scholar, Muday G.K. P.H. Plant and Google Scholar, C. Trends Plant Sci. 2002; Full Text Full Text PDF PubMed Scopus Google Scholar). roots of with flavonoid altered gravitropic and auxin are to the by of flavonoids (16Brown D.E. Rashotte A.M. Murphy A.S. Normanly J. Tague B.W. Peer W.A. Taiz L. Muday G.K. Plant Physiol. 2001; 126: 524-535Crossref PubMed Scopus (555) Google Scholar, Grotewold E. Curr. Plant Biol. 8: PubMed Scopus Google Scholar). the identity of the specific flavonoid compounds their molecular targets as as their of in vivo are essentially unknown. lines of that ABCBs are (8Blakeslee J.J. Bandyopadhyay A. Lee O.R. Mravec J. Titapiwatanakun B. Sauer M. Makam S.N. Cheng Y. Bouchard R. Adamec J. Geisler M. Nagashima A. Sakai T. Martinoia E. Friml J. Peer W.A. Murphy A.S. Plant Cell. 2007; 19: 131-147Crossref PubMed Scopus (326) Google Scholar, 9Lewis D.R. Miller N.D. Splitt B.L. Wu G. Spalding E.P. Plant Cell. 2007; 19: 1838-1850Crossref PubMed Scopus (151) Google Scholar, 10Wu G. Lewis D.R. Spalding E.P. Plant Cell. 2007; 19: 1826-1837Crossref PubMed Scopus (129) Google Scholar, R. A. Blakeslee J.J. Lee O.R. I. Palme K. S. Murphy A.S. B. Geisler M. J. Biol. 2006; Full Text Full Text PDF PubMed Scopus Google Scholar, M. Blakeslee J.J. Bouchard R. Lee O.R. Bandyopadhyay A. Titapiwatanakun B. Peer W.A. A. C. U. Muller A. R. Murphy A.S. Martinoia E. Plant J. PubMed Scopus Google Scholar) or A. D. D. B.W. S. Martinoia E. Geisler M. J. Biol. Full Text Full Text PDF PubMed Scopus Google Scholar) by concentrations inhibition of auxin efflux by R. A. Blakeslee J.J. Lee O.R. I. Palme K. S. Murphy A.S. B. Geisler M. J. Biol. 2006; Full Text Full Text PDF PubMed Scopus Google Scholar, M. Blakeslee J.J. Bouchard R. Lee O.R. Bandyopadhyay A. Titapiwatanakun B. Peer W.A. A. C. U. Muller A. R. Murphy A.S. Martinoia E. Plant J. PubMed Scopus Google Scholar), and D.R. Miller N.D. Splitt B.L. Wu G. Spalding E.P. Plant Cell. 2007; 19: 1838-1850Crossref PubMed Scopus (151) Google Scholar) to as probably by to the B. Murphy A.S. Spalding E.P. Plant Cell. 2001; PubMed Scopus Google Scholar). This is in to flavonoids, as inhibitors of plant R. A. Blakeslee J.J. Lee O.R. I. Palme K. S. Murphy A.S. B. Geisler M. J. Biol. 2006; Full Text Full Text PDF PubMed Scopus Google Scholar, M. Blakeslee J.J. Bouchard R. Lee O.R. Bandyopadhyay A. Titapiwatanakun B. Peer W.A. A. C. U. Muller A. R. Murphy A.S. Martinoia E. Plant J. PubMed Scopus Google Scholar, K. Blakeslee J.J. Titapiwatanakun B. Peer W.A. Bandyopadhyay A. Makam S.N. Lee O.R. Murphy A.S. K. Plant Cell. PubMed Scopus Google Scholar) and ABCBs S. Sci. 2006; PubMed Scopus Google Scholar), probably by and for G. G. D. A. Proc. Natl. Acad. Sci. U. S. A. 1998; 95: PubMed Scopus Google Scholar). In the and of PIN auxin efflux is to a of of auxin concentrations W.A. Bandyopadhyay A. Blakeslee J.J. Makam S.I. Chen R.J. Masson P.H. Murphy A.S. Plant Cell. 2004; 16: 1898-1911Crossref PubMed Scopus (305) Google Scholar, 19Peer W.A. Murphy A.S. Grotewold E. The Science of Flavonoids. Springer, Berlin2006: Scopus Google Scholar). In a that flavonoids are as that PIN and localization W.A. Bandyopadhyay A. Blakeslee J.J. Makam S.I. Chen R.J. Masson P.H. Murphy A.S. Plant Cell. 2004; 16: 1898-1911Crossref PubMed Scopus (305) Google Scholar). we that agravitropic pin2/eir1/wav6/agr1 has of flavonol glycosides. We that nanomolar concentrations of have apparently a root elongation and gravitropic response in partially the agravitropic of pin2 roots by asymmetric PIN1 polar auxin as and with a acid 2-aminoethyl and in Growth and Plant for in a and and in a for the with and with a The used in A. L. P. P. Marchant A. G. Bennett M. E. Palme K. EMBO J. 1998; PubMed Scopus Google Scholar) and C. P. Genes Dev. 1998; 12: PubMed Scopus Google Scholar). in vivo by the of compounds with for of to and Muday (14Buer C.S. Muday G.K. Plant Cell. 2004; 16: 1191-1205Crossref PubMed Scopus (312) Google Scholar). by with a and or with a of and roots in the in of and for The to and in of by a with a the The A for used as for with flow rate A and an with a an and an flow rate A and The to a with a The to the The and The in the in the mass from to The in the The the by and the in the The of flavonoid compounds as the of the of the mass during of a of of flavonoid compounds is the result of in root from from to with or or or to of and growth in the In of gravitropic of growth and of gravitropic from the of the gravity root to of the of the of the of root tip of root of and of and the of roots as root bending. of gravity stimulation by the for to the of flavonoid (14Buer C.S. Muday G.K. Plant Cell. 2004; 16: 1191-1205Crossref PubMed Scopus (312) Google Scholar). of gravity stimulation, roots and flavonoids as or of a of root and as in M. P.H. Science. PubMed Scopus Google gravitropic in the to responses. In and and of gravitropic in a to possible of pin2 roots gradients gravity stimulation as J. Benkova E. U. Palme K. G. Plant J. PubMed Scopus Google Scholar) with PIN1 specific T. E. N. J. J. N. G. N. Friml J. PubMed Scopus Google Scholar) and secondary of and out a In and of gradients and PIN1 distribution in a to possible pin2 an to as pin2 of the auxin transport basipetal auxin transport and agravitropic root growth R. Hilson P. Sedbrook J. Rosen E. Caspar T. Masson P.H. Proc. Natl. Acad. Sci. U. S. A. 1998; 95: 15112-15117Crossref PubMed Scopus (367) Google Scholar, A. L. P. P. Marchant A. G. Bennett M. E. Palme K. EMBO J. 1998; PubMed Scopus Google Scholar, C. P. Genes Dev. 1998; 12: PubMed Scopus Google Scholar, K. T. Y. T. Plant Cell Physiol. 1998; PubMed Scopus Google Scholar). a of we in basipetal auxin transport in result in agravitropic responses A.M. Muday G.K. 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Bandyopadhyay A. Blakeslee J.J. Makam S.I. Chen R.J. Masson P.H. Murphy A.S. Plant Cell. 2004; 16: 1898-1911Crossref PubMed Scopus (305) Google Scholar, W.A. D.E. Tague B.W. Muday G.K. Taiz L. Murphy A.S. Plant Physiol. 2001; 126: PubMed Scopus Google Scholar). flavonoid distribution by we and flavonoid in and pin2 and roots and with A and and we that the amount of flavonoids in the of pin2 and the root and pin2 roots altered of specific flavonol in the and in the root and in the of the of in and In pin2 roots and a from and flavonols to as that auxin may have an the or of This is by in of that are involved in flavonoid in T. Y. M. J. M. E. M. M. M. K. Plant J. PubMed Scopus Google Scholar). for a flavonoid is by acid and acid is by auxin transport inhibitor is in pin2 roots, may for the regulation of auxin transport during root in the of root and of and pin2 (14Buer C.S. Muday G.K. Plant Cell. 2004; 16: 1191-1205Crossref PubMed Scopus (312) Google Scholar, C.S. P. Muday G.K. 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Genes Dev. 1998; 12: PubMed Scopus Google Scholar), gravity for in the of pin2 gravitropic root by and A and of root by flavonols and The gravitropic in the of the inhibitor of polar auxin efflux NPA, basipetal from the root tip I. Marchant A. T. S. R. N. D. Sandberg G. Bennett M. Plant Cell. 2001; PubMed Scopus Google Scholar). In with NPA, a in an agravitropic (16Brown D.E. Rashotte A.M. Murphy A.S. Normanly J. Tague B.W. Peer W.A. Taiz L. Muday G.K. Plant Physiol. 2001; 126: 524-535Crossref PubMed Scopus (555) Google Scholar, A.M. Muday G.K. Plant Physiol. 2000; PubMed Scopus Google Scholar), to that for failed to restore pin2 root that of in pin2 lower concentrations or a as for a A.M. A. Muday G.K. Plant Cell. 2001; PubMed Scopus Google Scholar), we root of and pin2 with from to the used with the flavonols and a and not to restore root in in pin2 we in the of NPA, and that in NPA, an in pin2 the by that the of pin2 agravitropic response by is The of pin2 agravitropic root growth is a in the of auxin the lower side of the root elongation zone C. P. Genes Dev. 1998; 12: PubMed Scopus Google Scholar). We flavonoid the asymmetric auxin distribution necessary for differential growth of epidermal cells during gravitropic responses. This by the auxin I. P. C. Sandberg G. M. Palme K. Proc. Natl. Acad. Sci. U. S. A. PubMed Scopus Google Scholar), in with roots, the in specific cell and localized in the in the and in the cells pin2 roots a in the lateral root cap with the lateral root a in basipetal auxin In roots with or in essentially to the in the and pin2 a gravity stimulation, fluorescent in roots in the lower in the lateral root cap and EZ, in controls in the of flavonoids In flavonoid of pin2 roots in a of a asymmetric in the lateral root cap with the lower of the root and the of the root asymmetric auxin gravity stimulation, we determined root auxin symmetry from to in to their tip to the gravity stimulation to of and and with the of pin2 a auxin distribution of auxin symmetry asymmetric auxin gradients as of of symmetry in pin2 gravity stimulation is in with the of the gravitropic a of auxin gradients in pin2 in roots not in the The of the lower and side in pin2 roots in the elongation zone and in the of the roots with In a with auxin gradients apparently result in gravitropic responses in roots, of class roots auxin to lateral root the number of roots an asymmetric to This number to that of the roots gravitropic responses show that flavonoids are to the asymmetric in the pin2 roots the for of gravitropic responses. PIN1 of PIN have been demonstrated A. S. Wisniewska J. Benkova E. Benjamins R. T. Luschnig C. Friml J. PubMed Scopus Google Scholar, I. Xu J. M. I. Friml J. R. M. Palme K. Scheres B. PubMed Scopus Google Scholar), we the root gravitropic responses of the pin2 in the of A agravitropic root for pin2 in I. Xu J. M. I. Friml J. R. M. Palme K. Scheres B. PubMed Scopus Google Scholar), partially by the of with or not we that are for of the agravitropic response of with their and in gravity tissues I. Xu J. M. I. Friml J. R. M. Palme K. Scheres B. PubMed Scopus Google Scholar). we the gravitropic with roots of the not agravitropic with demonstrate that PIN1 is for complementation of pin2 is in with in gravity or response the of PIN1 during pin2 gravitropic responses and to a possible the of flavonoids and PIN1 in we PIN1 localization in pin2 roots to and during a gravity with A. S. Wisniewska J. Benkova E. Benjamins R. T. Luschnig C. Friml J. PubMed Scopus Google Scholar, I. Xu J. M. I. Friml J. R. M. Palme K. Scheres B. PubMed Scopus Google Scholar), in roots PIN1 the of and cells with in the and In pin2 roots, PIN1 in the apical localization in the and localization in cells in A. S. Wisniewska J. Benkova E. Benjamins R. T. Luschnig C. Friml J. PubMed Scopus Google Scholar). This PIN1 altered by a gravity of roots with the distribution of PIN1 and as W.A. Bandyopadhyay A. Blakeslee J.J. Makam S.I. Chen R.J. Masson P.H. Murphy A.S. Plant Cell. 2004; 16: 1898-1911Crossref PubMed Scopus (305) Google Scholar) not symmetry of in in pin2 roots In gravity stimulation of pin2 roots in the of in asymmetric of PIN1 with the lower side of the root tip The of PIN1 gradients with the of asymmetric in the absence of asymmetric PIN1 with asymmetric We asymmetric gradients that with PIN1 or gradients with asymmetric PIN1 for a roots we a asymmetric PIN1 and The in auxin is that flavonoids act as of by accumulating in the epidermal cells of the root elongation zone (14Buer C.S. Muday G.K. Plant Cell. 2004; 16: 1191-1205Crossref PubMed Scopus (312) Google Scholar, D.E. Rashotte A.M. Murphy A.S. Normanly J. Tague B.W. Peer W.A. Taiz L. Muday G.K. Plant Physiol. 2001; 126: 524-535Crossref PubMed Scopus (555) Google Scholar, 17Murphy A. Peer W.A. Taiz L. Planta. 2000; 211: 315-324Crossref PubMed Scopus (282) Google Scholar, 18Peer W.A. Bandyopadhyay A. Blakeslee J.J. Makam S.I. Chen R.J. Masson P.H. Murphy A.S. Plant Cell. 2004; 16: 1898-1911Crossref PubMed Scopus (305) Google Scholar, 19Peer W.A. Murphy A.S. Grotewold E. The Science of Flavonoids. Springer, Berlin2006: Scopus Google Scholar, W.A. D.E. Tague B.W. Muday G.K. Taiz L. Murphy A.S. Plant Physiol. 2001; 126: PubMed Scopus Google Scholar). demonstrate that in basipetal auxin transport are associated with altered root flavonoid In in auxin transport is synthesis and of specific flavonoid in the root tip elongation not the root or in the are and and and pin2 roots the to flavonoids in response to a gravity not as as the Application of concentrations of flavonoids partially gravitropic root tip in a in basipetal auxin transport and of flavonoid is apparently from that of that gravity stimulation of pin2 roots in the of a of shown to A. D. D. B.W. S. Martinoia E. Geisler M. J. Biol. Full Text Full Text PDF PubMed Scopus Google Scholar, A.M. Muday G.K. Plant Physiol. 2000; PubMed Scopus Google Scholar, A.M. A. Muday G.K. Plant Cell. 2001; PubMed Scopus Google Scholar) not pin2 that in and concentrations of flavonoids not act as cell of show that complementation of by flavonoids is by of asymmetric distribution of in the pin2 This that of gravitropic responses is the of an thus the of a for basipetal auxin of root gravitropic response of that PIN1 is for complementation of pin2 is in with in gravity or response a quantitative cell biological approach, we that of pin2 by PIN1 is with asymmetric PIN1 distribution In that PIN1 is the auxin efflux that basipetal auxin for gravitropic responses in pin2 The PIN1 shifts in pin2 roots are in with the that PIN1 and have in the root I. Xu J. M. I. Friml J. R. M. Palme K. Scheres B. PubMed Scopus Google Scholar) and that PIN1 and localized the side of epidermal cells J. Xu J. Seifertova D. Brewer P.B. Ruzicka K. Blilou I. Rouquie D. Benkova E. Scheres B. Friml J. Science. 2006; 312: 883Crossref PubMed Scopus (662) Google Scholar). PIN1 a apical localization in and localization in cells in roots of pin2 A. S. Wisniewska J. Benkova E. Benjamins R. T. Luschnig C. Friml J. PubMed Scopus Google Scholar). that flavonoids are the that promote asymmetric PIN1 shifts with the lower side of the root tip in response to a gravity thus redirecting basipetal auxin streams necessary for root tip bending. The that flavonols and from their has to the that flavonoids and act targets lines of that plant and are targets of flavonoid regulation (8Blakeslee J.J. Bandyopadhyay A. Lee O.R. Mravec J. Titapiwatanakun B. Sauer M. Makam S.N. Cheng Y. Bouchard R. Adamec J. Geisler M. Nagashima A. Sakai T. Martinoia E. Friml J. Peer W.A. Murphy A.S. Plant Cell. 2007; 19: 131-147Crossref PubMed Scopus (326) Google Scholar, R. A. Blakeslee J.J. Lee O.R. I. Palme K. S. Murphy A.S. B. Geisler M. J. Biol. 2006; Full Text Full Text PDF PubMed Scopus Google Scholar, M. Blakeslee J.J. Bouchard R. Lee O.R. Bandyopadhyay A. Titapiwatanakun B. Peer W.A. A. C. U. Muller A. R. Murphy A.S. Martinoia E. Plant J. PubMed Scopus Google Scholar) M. P.H. Science. PubMed Scopus Google Scholar), or inhibition of or in to ABCBs G. G. D. A. Proc. Natl. Acad. Sci. U. S. A. 1998; 95: PubMed Scopus Google Scholar). This of flavonoids by the of flavonoids of the PIN family has and to and result in of auxin streams W.A. Bandyopadhyay A. Blakeslee J.J. Makam S.I. Chen R.J. Masson P.H. Murphy A.S. Plant Cell. 2004; 16: 1898-1911Crossref PubMed Scopus (305) Google Scholar, W.A. Murphy A.S. Trends Plant Sci. 2007; 12: Full Text Full Text PDF PubMed Scopus Google Scholar) and by In with we lines of that flavonoids, not efflux are to function as of polar auxin flavonoid concentrations to the roots not and not a failed to restore pin2 root of pin2 agravitropic response by that flavonoids promote PIN1 shifts in response to a gravity an of flavonoids in cellular of auxin transport components as suggested W.A. Bandyopadhyay A. Blakeslee J.J. Makam S.I. Chen R.J. Masson P.H. Murphy A.S. Plant Cell. 2004; 16: 1898-1911Crossref PubMed Scopus (305) Google Scholar, W.A. Murphy A.S. Trends Plant Sci. 2007; 12: Full Text Full Text PDF PubMed Scopus Google Scholar). The of in pin2 by flavonoid the of basipetal auxin transport (16Brown D.E. Rashotte A.M. Murphy A.S. Normanly J. Tague B.W. Peer W.A. Taiz L. Muday G.K. Plant Physiol. 2001; 126: 524-535Crossref PubMed Scopus (555) Google Scholar, 17Murphy A. Peer W.A. Taiz L. Planta. 2000; 211: 315-324Crossref PubMed Scopus (282) Google Scholar) and root of (14Buer C.S. Muday G.K. Plant Cell. 2004; 16: 1191-1205Crossref PubMed Scopus (312) Google Scholar) by of flavonoids and are with a of flavonoids in gravitropic a and flavonoids, the flavonoid flavonoid synthesis (16Brown D.E. Rashotte A.M. Murphy A.S. Normanly J. Tague B.W. Peer W.A. Taiz L. Muday G.K. Plant Physiol. 2001; 126: 524-535Crossref PubMed Scopus (555) Google Scholar, W.A. Murphy A.S. Trends Plant Sci. 2007; 12: Full Text Full Text PDF PubMed Scopus Google Scholar). these and the used the or of flavonoids auxin This partially by from Peer W.A. Bandyopadhyay A. Blakeslee J.J. Makam S.I. Chen R.J. Masson P.H. Murphy A.S. Plant Cell. 2004; 16: 1898-1911Crossref PubMed Scopus (305) Google Scholar) that regulation of and PIN1 by is in the absence of flavonoids, PIN1 is PIN1 is from the in the absence of flavonoids, is not W.A. Bandyopadhyay A. Blakeslee J.J. Makam S.I. Chen R.J. Masson P.H. Murphy A.S. Plant Cell. 2004; 16: 1898-1911Crossref PubMed Scopus (305) Google Scholar). This that flavonoids act as of as of The that auxin PIN1 in the that the by PIN1 is in the pin2 lower auxin in these cells that are for basipetal auxin in that of root by flavonoids may result from a of regulation and PIN that and Although the cellular targets of flavonoid are the with PIN that flavonoids probably not with flavonoids specific PIN and cellular probably with W.A. Bandyopadhyay A. Blakeslee J.J. Makam S.I. Chen R.J. Masson P.H. Murphy A.S. Plant Cell. 2004; 16: 1898-1911Crossref PubMed Scopus (305) Google Scholar, W.A. Murphy A.S. Trends Plant Sci. 2007; 12: Full Text Full Text PDF PubMed Scopus Google Scholar). PIN shifts have been demonstrated to by PIN and J. M. D. A. Benjamins R. P.B. Ljung K. Sandberg G. Palme K. R. Science. 2004; PubMed Scopus Google Scholar, M. L. D. A. I. C. J. R. D. Luschnig C. R. Friml J. Cell. 2007; Full Text Full Text PDF PubMed Scopus Google Scholar). with the that flavonols are used as and inhibitors or J.C. Plant J. 2006; PubMed Scopus Google Scholar) the targets for We for and and for flavonol that for the flavonol M. for during the root and and S. for the with