7-Rhamnosylated Flavonols Modulate Homeostasis of the Plant Hormone Auxin and Affect Plant Development

. 2016 Mar 04 ; 291 (10) : 5385-95. [epub] 20160107

Jazyk angličtina Země Spojené státy americké Médium print-electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid26742840
Odkazy

PubMed 26742840
PubMed Central PMC4777868
DOI 10.1074/jbc.m115.701565
PII: S0021-9258(20)43172-2
Knihovny.cz E-zdroje

Flavonols are a group of secondary metabolites that affect diverse cellular processes. They are considered putative negative regulators of the transport of the phytohormone auxin, by which they influence auxin distribution and concomitantly take part in the control of plant organ development. Flavonols are accumulating in a large number of glycosidic forms. Whether these have distinct functions and diverse cellular targets is not well understood. The rol1-2 mutant of Arabidopsis thaliana is characterized by a modified flavonol glycosylation profile that is inducing changes in auxin transport and growth defects in shoot tissues. To determine whether specific flavonol glycosides are responsible for these phenotypes, a suppressor screen was performed on the rol1-2 mutant, resulting in the identification of an allelic series of UGT89C1, a gene encoding a flavonol 7-O-rhamnosyltransferase. A detailed analysis revealed that interfering with flavonol rhamnosylation increases the concentration of auxin precursors and auxin metabolites, whereas auxin transport is not affected. This finding provides an additional level of complexity to the possible ways by which flavonols influence auxin distribution and suggests that flavonol glycosides play an important role in regulating plant development.

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Lepiniec L., Debeaujon I., Routaboul J. M., Baudry A., Pourcel L., Nesi N., and Caboche M. (2006) Genetics and biochemistry of seed flavonoids. Annu. Rev. Plant Biol. 57, 405–430 PubMed

Costa D., Galvao A. M., Di Paolo R. E., Freitas A. A., Lima J. C., Quina F. H., and Macanita A. L. (2015) Photochemistry of the hemiketal form of anthocyanins and its potential role in plant protection from UV-B radiation. Tetrahedron 71, 3157–3162

Zhang J., Subramanian S., Stacey G., and Yu O. (2009) Flavones and flavonols play distinct critical roles during nodulation of Medicago truncatula by Sinorhizobium meliloti. Plant J. 57, 171–183 PubMed

Brown J. E., Khodr H., Hider R. C., and Rice-Evans C. A. (1998) Structural dependence of flavonoid interactions with Cu2+ ions: implications for their antioxidant properties. Biochem. J. 330, 1173–1178 PubMed PMC

Taylor L. P., and Grotewold E. (2005) Flavonoids as developmental regulators. Curr. Opin. Plant Biol. 8, 317–323 PubMed

Mo Y. Y., Nagel C., and Taylor L. P. (1992) Biochemical complementation of chalcone synthase mutants defines a role for flavonols in functional pollen. Proc. Natl. Acad. Sci. U.S.A. 89, 7213–7217 PubMed PMC

Peer W. A., and Murphy A. S. (2006) Flavonoids as signal molecules. in The Science of Flavonoids (Grotewold E. ed), pp. 239–268, Springer-Verlag, Berlin

Yin R., Messner B., Faus-Kessler T., Hoffmann T., Schwab W., Hajirezaei M.-R., von Saint Paul V., Heller W., and Schäffner A. R. (2012) Feedback inhibition of the general phenylpropanoid and flavonol biosynthetic pathways upon a compromised flavonol-3-O-glycosylation. J. Exp. Bot. 63, 2465–2478 PubMed PMC

Nakabayashi R., Yonekura-Sakakibara K., Urano K., Suzuki M., Yamada Y., Nishizawa T., Matsuda F., Kojima M., Sakakibara H., Shinozaki K., Michael A. J., Tohge T., Yamazaki M., and Saito K. (2014) Enhancement of oxidative and drought tolerance in Arabidopsis by overaccumulation of antioxidant flavonoids. Plant J. 77, 367–379 PubMed PMC

Jacobs M., and Rubery P. H. (1988) Naturally-occurring auxin transport regulators. Science 241, 346–349 PubMed

Buer C. S., and Muday G. K. (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 PubMed PMC

Brown D. E., Rashotte A. M., Murphy A. S., Normanly J., Tague B. W., Peer W. A., Taiz L., and Muday G. K. (2001) Flavonoids act as negative regulators of auxin transport in vivo in Arabidopsis. Plant Physiol. 126, 524–535 PubMed PMC

Peer W. A., Bandyopadhyay A., Blakeslee J. J., Makam S. N., Chen R. J., Masson P. H., and Murphy A. S. (2004) Variation in expression and protein localization of the PIN family of auxin efflux facilitator proteins in flavonoid mutants with altered auxin transport in Arabidopsis thaliana. Plant Cell 16, 1898–1911 PubMed PMC

Peer W. A., Blakeslee J. J., Yang H., and Murphy A. S. (2011) Seven things we think we know about auxin transport. Mol. Plant 4, 487–504 PubMed

Zažímalová E., Murphy A. S., Yang H., Hoyerová K., and Hosek P. (2010) Auxin transporters: why so many? Cold Spring Harb. Perspect. Biol. 2, a001552. PubMed PMC

Remmer J., and Murphy A. S. (2014) Intercellular transport of auxin. in Auxin and its role in plant development (Zažímalová E., Petrášek J., and Benková E. eds.), pp. 75–100, Springer, Vienna

Bouchard R., Bailly A., Blakeslee J. J., Oehring S. C., Vincenzetti V., Lee O. R., Paponov I., Palme K., Mancuso S., Murphy A. S., Schulz B., and Geisler M. (2006) Immunophilin-like TWISTED DWARF1 modulates auxin efflux activities of Arabidopsis P-glycoproteins. J. Biol. Chem. 281, 30603–30612 PubMed

Bailly A., Sovero V., Vincenzetti V., Santelia D., Bartnik D., Koenig B. W., Mancuso S., Martinoia E., and Geisler M. (2008) Modulation of P-glycoproteins by auxin transport inhibitors is mediated by interaction with immunophilins. J. Biol. Chem. 283, 21817–21826 PubMed

Michniewicz M., Zago M. K., Abas L., Weijers D., Schweighofer A., Meskiene I., Heisler M. G., Ohno C., Zhang J., Huang F., Schwab R., Weigel D., Meyerowitz E. M., Luschnig C., Offringa R., and Friml J. (2007) Antagonistic regulation of PIN phosphorylation by PP2A and PINOID directs auxin flux. Cell 130, 1044–1056 PubMed

Henrichs S., Wang B., Fukao Y., Zhu J., Charrier L., Bailly A., Oehring S. C., Linnert M., Weiwad M., Endler A., Nanni P., Pollmann S., Mancuso S., Schulz A., and Geisler M. (2012) Regulation of ABCB1/PGP1-catalysed auxin transport by linker phosphorylation. EMBO J. 31, 2965–2980 PubMed PMC

Chen R., Hilson P., Sedbrook J., Rosen E., Caspar T., and Masson P. H. (1998) The Arabidopsis thaliana AGRAVITROPIC 1 gene encodes a component of the polar-auxin-transport efflux carrier. Proc. Natl. Acad. Sci. U.S.A. 95, 15112–15117 PubMed PMC

Luschnig C., Gaxiola R. A., Grisafi P., and Fink G. R. (1998) EIR1, a root-specific protein involved in auxin transport, is required for gravitropism in Arabidopsis thaliana. Genes Dev. 12, 2175–2187 PubMed PMC

Santelia D., Henrichs S., Vincenzetti V., Sauer M., Bigler L., Klein M., Bailly A., Lee Y., Friml J., Geisler M., and Martinoia E. (2008) Flavonoids redirect PIN-mediated polar auxin fluxes during root gravitropic responses. J. Biol. Chem. 283, 31218–31226 PubMed PMC

Koornneef M. (1990) Mutations affecting the testa color in Arabidopsis. Arab. Inf. Serv. 19, 113–115

Routaboul J. M., Kerhoas L., Debeaujon I., Pourcel L., Caboche M., Einhorn J., and Lepiniec L. (2006) Flavonoid diversity and biosynthesis in seed of Arabidopsis thaliana. Planta 224, 96–107 PubMed

Yonekura-Sakakibara K., Tohge T., Matsuda F., Nakabayashi R., Takayama H., Niida R., Watanabe-Takahashi A., Inoue E., and Saito K. (2008) Comprehensive flavonol profiling and transcriptome coexpression analysis leading to decoding gene-metabolite correlations in Arabidopsis. Plant Cell 20, 2160–2176 PubMed PMC

Jones P., Messner B., Nakajima J., Schäffner A. R., and Saito K. (2003) UGT73C6 and UGT78D1, glycosyltransferases involved in flavonol glycoside biosynthesis in Arabidopsis thaliana. J. Biol. Chem. 278, 43910–43918 PubMed

Tohge T., Nishiyama Y., Hirai M. Y., Yano M., Nakajima J., Awazuhara M., Inoue E., Takahashi H., Goodenowe D. B., Kitayama M., Noji M., Yamazaki M., and Saito K. (2005) Functional genomics by integrated analysis of metabolome and transcriptome of Arabidopsis plants over-expressing an MYB transcription factor. Plant J. 42, 218–235 PubMed

Yonekura-Sakakibara K., Tohge T., Niida R., and Saito K. (2007) Identification of a flavonol 7-O-rhamnosyltransferase gene determining flavonoid pattern in Arabidopsis by transcriptome coexpression analysis and reverse genetics. J. Biol. Chem. 282, 14932–14941 PubMed

Ringli C., Bigler L., Kuhn B. M., Leiber R. M., Diet A., Santelia D., Frey B., Pollmann S., and Klein M. (2008) The modified flavonol glycosylation profile in the Arabidopsis rol1 mutants results in alterations in plant growth and cell shape formation. Plant Cell 20, 1470–1481 PubMed PMC

Yin R., Han K., Heller W., Albert A., Dobrev P. I., Zažímalová E., and Schäffner A. R. (2014) Kaempferol 3-O-rhamnoside-7-O-rhamnoside is an endogenous flavonol inhibitor of polar auxin transport in Arabidopsis shoots. New Phytol. 201, 466–475 PubMed PMC

Ostin A., Kowalyczk M., Bhalerao R. P., and Sandberg G. (1998) Metabolism of indole-3-acetic acid in Arabidopsis. Plant Physiol. 118, 285–296 PubMed PMC

Tam Y. Y., Epstein E., and Normanly J. (2000) Characterization of auxin conjugates in Arabidopsis: low steady-state levels of indole-9-acetyl-aspartate indole-3-acetyl-glutamate, and indole-3-acetyl-glucose. Plant Physiol. 123, 589–596 PubMed PMC

Korasick D. A., Enders T. A., and Strader L. C. (2013) Auxin biosynthesis and storage forms. J. Exp. Bot. 64, 2541–2555 PubMed PMC

Novák O., Hényková E., Sairanen I., Kowalczyk M., Pospíšil T., and Ljung K. (2012) Tissue-specific profiling of the Arabidopsis thaliana auxin metabolome. Plant J. 72, 523–536 PubMed

Kai K., Horita J., Wakasa K., and Miyagawa H. (2007) Three oxidative metabolites of indole-3-acetic acid from Arabidopsis thaliana. Phytochemistry 68, 1651–1663 PubMed

Pencík A., Simonovik B., Petersson S. V., Henyková E., Simon S., Greenham K., Zhang Y., Kowalczyk M., Estelle M., Zažímalová E., Novák O., Sandberg G., and Ljung K. (2013) Regulation of auxin homeostasis and gradients in Arabidopsis roots through the formation of the indole-3-acetic acid catabolite 2-oxindole-3-acetic acid. Plant Cell 25, 3858–3870 PubMed PMC

Benjamins R., and Scheres B. (2008) Auxin: the looping star in plant development. Annu. Rev. Plant Biol. 59, 443–465 PubMed

Vanneste S., and Friml J. (2009) Auxin: a trigger for change in plant development. Cell 136, 1005–1016 PubMed

Habets M. E. J., and Offringa R. (2014) PIN-driven polar auxin transport in plant developmental plasticity: a key target for environmental and endogenous signals. New Phytol. 203, 362–377 PubMed

Runions A., Smith R., and Prusinkiewicz P. (2014) Computational models of auxin-driven development. in Auxin and its role in plant development (Zažímalová E., Petrášek J., and Benková E. eds.), Springer, Vienna: pp 315–357

Peer W. A., Cheng Y., and Murphy A. S. (2013) Evidence of oxidative attenuation of auxin signalling. J. Exp. Bot. 64, 2629–2639 PubMed

Diet A., Link B., Seifert G. J., Schellenberg B., Wagner U., Pauly M., Reiter W. D., and Ringli C. (2006) The Arabidopsis root hair cell wall formation mutant lrx1 is suppressed by mutations in the RHM1 gene encoding a UDP-l-rhamnose synthase. Plant Cell 18, 1630–1641 PubMed PMC

Kuhn B. M., Geisler M., Bigler L., and Ringli C. (2011) Flavonols accumulate asymmetrically and affect auxin transport in Arabidopsis. Plant Physiol. 156, 585–595 PubMed PMC

Reiter W. D., and Vanzin G. F. (2001) Molecular genetics of nucleotide sugar interconversion pathways in plants. Plant. Mol. Biol. 47, 95–113 PubMed

Leiber R.-M., John F., Verhertbruggen Y., Diet A., Knox J. P., and Ringli C. (2010) The TOR pathway modulates the structure of cell walls in Arabidopsis. Plant Cell 22, 1898–1908 PubMed PMC

Stintzi A., and Browse J. (2000) The Arabidopsis male-sterile mutant, opr3, lacks the 12-oxophytodienoic acid reductase required for jasmonate synthesis. Proc. Natl. Acad. Sci. U.S.A. 97, 10625–10630 PubMed PMC

Horiguchi G., Fujikura U., Ferjani A., Ishikawa N., and Tsukaya H. (2006) Large-scale histological analysis of leaf mutants using two simple leaf observation methods: identification of novel genetic pathways governing the size and shape of leaves. Plant J. 48, 638–644 PubMed

Geisler M., Blakeslee J. J., Bouchard R., Lee O. R., Vincenzetti V., Bandyopadhyay A., Titapiwatanakun B., Peer W. A., Bailly A., Richards E. L., Ejenda K. F. K., Smith A. P., Baroux C., Grossniklaus U., Müller A., Hrycyna C. A., Dudler R., Murphy A. S., and Martinoia E. (2005) Cellular efflux of auxin catalyzed by the Arabidopsis MDR/PGP transporter AtPGP1. Plant J. 44, 179–194 PubMed

Geisler M., Kolukisaoglu H. U., Bouchard R., Billion K., Berger J., Saal B., Frangne N., Koncz-Kalman Z., Koncz C., Dudler R., Blakeslee J. J., Murphy A. S., Martinoia E., and Schulz B. (2003) TWISTED DWARF1, a unique plasma membrane-anchored immunophilin-like protein, interacts with Arabidopsis multidrug resistance-like transporters AtPGP1 and AtPGP19. Mol. Biol. Cell 14, 4238–4249 PubMed PMC

Lewis D. R., and Muday G. K. (2009) Measurement of auxin transport in Arabidopsis thaliana. Nat. Protoc. 4, 437–451 PubMed

Dobrev P. I., and Kamínek M. (2002) Fast and efficient separation of cytokinins from auxin and abscisic acid and their purification using mixed-mode solid-phase extraction. J. Chromatogr. A 950, 21–29 PubMed

Dobrev P. I., and Vankova R. (2012) Quantification of abscisic acid, cytokinin, and auxin content in salt-stressed plant tissues. Methods Mol. Biol. 913, 251–261 PubMed

Shao H., He X., Achnine L., Blount J. W., Dixon R. A., and Wang X. (2005) Crystal structures of a multifunctional triterpene/flavonoid glycosyltransferase from Medicago truncatula. Plant Cell 17, 3141–3154 PubMed PMC

Offen W., Martinez-Fleites C., Yang M., Kiat-Lim E., Davis B. G., Tarling C. A., Ford C. M., Bowles D. J., and Davies G. J. (2006) Structure of a flavonoid glucosyltransferase reveals the basis for plant natural product modification. EMBO J. 25, 1396–1405 PubMed PMC

Osmani S. A., Bak S., and Møller B. L. (2009) Substrate specificity of plant UDP-dependent glycosyltransferases predicted from crystal structures and homology modeling. Phytochemistry 70, 325–347 PubMed

Butelli E., Titta L., Giorgio M., Mock H.-P., Matros A., Peterek S., Schijlen E. G. W. M., Hall R. D., Bovy A. G., Luo J., and Martin C. (2008) Enrichment of tomato fruit with health-promoting anthocyanins by expression of select transcription factors. Nat. Biotechnol. 26, 1301–1308 PubMed

Buer C. S., Kordbacheh F., Truong T. T., Hocart C. H., and Djordjevic M. A. (2013) Alteration of flavonoid accumulation patterns in transparent testa mutants disturbs auxin transport, gravity responses, and imparts long-term effects on root and shoot architecture. Planta 238, 171–189 PubMed

Lewis D. R., Ramirez M. V., Miller N. D., Vallabhaneni P., Ray W. K., Helm R. F., Winkel B. S. J., and Muday G. K. (2011) Auxin and ethylene induce flavonol accumulation through distinct transcriptional networks. Plant Physiol. 156, 144–164 PubMed PMC

Woodward A. W., and Bartel B. (2005) Auxin: Regulation, action, and interaction. Ann. Bot. 95, 707–735 PubMed PMC

Rampey R. A., LeClere S., Kowalczyk M., Ljung K., Sandberg G., and Bartel B. (2004) A family of auxin-conjugate hydrolases that contributes to free indole-3-acetic acid levels during Arabidopsis germination. Plant Physiol. 135, 978–988 PubMed PMC

Spiess G. M., Hausman A., Yu P., Cohen J. D., Rampey R. A., and Zolman B. K. (2014) Auxin input pathway disruptions are mitigated by changes in auxin biosynthetic gene expression in Arabidopsis. Plant Physiol. 165, 1092–1104 PubMed PMC

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