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• W3115804594 abstract "Flavonoids are a class of specialized metabolites with subclasses including flavonols and anthocyanins, which have unique properties as antioxidants. Flavonoids modulate plant development, but whether and how they impact lateral root development is unclear. We examined potential roles for flavonols in this process using Arabidopsis thaliana mutants with defects in genes encoding key enzymes in flavonoid biosynthesis. We observed the tt4 and fls1 mutants, which produce no flavonols, have increased lateral root emergence. The tt4 root phenotype was reversed by genetic and chemical complementation. To more specifically define the flavonoids involved, we tested an array of flavonoid biosynthetic mutants, eliminating roles for anthocyanins and the flavonols quercetin and isorhamnetin in modulating lateral root development. Instead, two tt7 mutant alleles, with defects in a branchpoint enzyme blocking quercetin biosynthesis, formed reduced numbers of lateral roots and tt7-2 had elevated levels of kaempferol. Using a flavonol-specific dye, we observed that in the tt7-2 mutant, kaempferol accumulated within lateral root primordia at higher levels than wild-type. These data are consistent with kaempferol, or downstream derivatives, acting as a negative regulator of lateral root emergence. We examined ROS accumulation using ROS-responsive probes and found reduced fluorescence of a superoxide-selective probe within the primordia of tt7-2 compared with wild-type, but not in the tt4 mutant, consistent with opposite effects of these mutants on lateral root emergence. These results support a model in which increased level of kaempferol in the lateral root primordia of tt7-2 reduces superoxide concentration and ROS-stimulated lateral root emergence. Flavonoids are a class of specialized metabolites with subclasses including flavonols and anthocyanins, which have unique properties as antioxidants. Flavonoids modulate plant development, but whether and how they impact lateral root development is unclear. We examined potential roles for flavonols in this process using Arabidopsis thaliana mutants with defects in genes encoding key enzymes in flavonoid biosynthesis. We observed the tt4 and fls1 mutants, which produce no flavonols, have increased lateral root emergence. The tt4 root phenotype was reversed by genetic and chemical complementation. To more specifically define the flavonoids involved, we tested an array of flavonoid biosynthetic mutants, eliminating roles for anthocyanins and the flavonols quercetin and isorhamnetin in modulating lateral root development. Instead, two tt7 mutant alleles, with defects in a branchpoint enzyme blocking quercetin biosynthesis, formed reduced numbers of lateral roots and tt7-2 had elevated levels of kaempferol. Using a flavonol-specific dye, we observed that in the tt7-2 mutant, kaempferol accumulated within lateral root primordia at higher levels than wild-type. These data are consistent with kaempferol, or downstream derivatives, acting as a negative regulator of lateral root emergence. We examined ROS accumulation using ROS-responsive probes and found reduced fluorescence of a superoxide-selective probe within the primordia of tt7-2 compared with wild-type, but not in the tt4 mutant, consistent with opposite effects of these mutants on lateral root emergence. These results support a model in which increased level of kaempferol in the lateral root primordia of tt7-2 reduces superoxide concentration and ROS-stimulated lateral root emergence. Flavonoids are a class of plant specialized metabolites with important functions in modulating development and stress responses (1Chapman J.M. Muhlemann J.K. Gayomba S.R. Muday G.K. RBOH-Dependent ROS synthesis and ROS scavenging by plant specialized metabolites to modulate plant development and stress responses.Chem. Res. Toxicol. 2019; 32: 370-396Crossref PubMed Scopus (50) Google Scholar, 2Gayomba S.R. Watkins J.M. Muday G.K. Flavonols regulate plant growth and development through regulation of auxin transport and cellular redox status.in: Yoshidaessor K. Director V.C.R. Quideauessor S. Recent Advances in Polyphenol Research. John Wiley & Sons, Ltd, 2017: 143-170Crossref Scopus (14) Google Scholar). There are multiple subclasses of flavonoids including chalcones, flavones, isoflavonoids, flavanones, flavonols, and anthocyanins (3Winkel-Shirley B. Flavonoid biosynthesis. A colorful model for genetics, biochemistry, cell biology, and biotechnology.Plant Physiol. 2001; 126: 485-493Crossref PubMed Scopus (2201) Google Scholar). The pathway begins with the conversion of 4-Coumaroyl CoA and Malonyl CoA to naringenin chalcone. Further downstream, dihydroflavonols are produced and can be converted to either flavonols or anthocyanins. Flavonols and anthocyanins are two of the best studied flavonoid subclasses due to their ubiquitous presence in multiple species, their diverse functionality (4Panche A.N. Diwan A.D. Chandra S.R. Flavonoids: an overview.J. Nutr. Sci. 2016; 5: e47Crossref PubMed Scopus (1213) Google Scholar), and antioxidant capacity (5Agati G. Azzarello E. Pollastri S. Tattini M. Flavonoids as antioxidants in plants: location and functional significance.Plant Sci. 2012; 196: 67-76Crossref PubMed Scopus (909) Google Scholar, 6Csepregi K. Hideg É. Phenolic compound diversity explored in the context of photo-oxidative stress protection.Phytochem. Anal. 2018; 29: 129-136Crossref PubMed Scopus (33) Google Scholar, 7Pietta P.-G. Flavonoids as antioxidants.J. Nat. Prod. 2000; 63: 1035-1042Crossref PubMed Scopus (3266) Google Scholar, 8Heim K.E. Tagliaferro A.R. Bobilya D.J. Flavonoid antioxidants: chemistry, metabolism and structure-activity relationships.J. Nutr. Biochem. 2002; 13: 572-584Crossref PubMed Scopus (2690) Google Scholar). Arabidopsis thaliana synthesizes three flavonols: kaempferol, quercetin, and isorhamnetin, which differ by the presence of a hydroxyl or methoxy group on their ring. The flavonoid biosynthesis pathway is well characterized in Arabidopsis with mutants isolated in the genes encoding each of the enzymes of the biosynthetic pathway (3Winkel-Shirley B. Flavonoid biosynthesis. A colorful model for genetics, biochemistry, cell biology, and biotechnology.Plant Physiol. 2001; 126: 485-493Crossref PubMed Scopus (2201) Google Scholar). Flavonoid biosynthetic mutants have been used to better understand the role of flavonols as signaling molecules that modulate development. The Arabidopsis transparent testa 4 (tt4) mutant produces no flavonoids due to a mutation in the gene encoding the enzyme catalyzing the first committed step in the flavonoid biosynthesis pathway, chalcone synthase (CHS). Previous studies showed that tt4 has increased root hair formation (9Gayomba S.R. Muday G.K. Flavonols regulate root hair development by modulating accumulation of reactive oxygen species in the root epidermis.Development. 2020; 147dev185819Crossref PubMed Google Scholar), ABA-induced stomatal closure (10Watkins J.M. Hechler P.J. Muday G.K. Ethylene-induced flavonol accumulation in guard cells suppresses reactive oxygen species and moderates stomatal aperture.Plant Physiol. 2014; 164: 1707-1717Crossref PubMed Scopus (111) Google Scholar), impaired gravity response (11Lewis D.R. Ramirez M.V. Miller N.D. Vallabhaneni P. Ray W.K. Helm R.F. Winkel B.S.J. Muday G.K. Auxin and ethylene induce flavonol accumulation through distinct transcriptional networks.Plant Physiol. 2011; 156: 144-164Crossref PubMed Scopus (166) Google Scholar), and greater sensitivity to environmental stress (12Nakabayashi 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. Saito K. Enhancement of oxidative and drought tolerance in Arabidopsis by overaccumulation of antioxidant flavonoids.Plant J. 2014; 77: 367-379Crossref PubMed Scopus (468) Google Scholar). Additional pathway mutants have been used to reveal which flavonols function in development, including identification of specific kaempferol derivatives that regulate leaf shape (13Ringli C. Bigler L. Kuhn B.M. Leiber R.-M. Diet A. Santelia D. Frey B. Pollmann S. Klein M. The modified flavonol glycosylation profile in the Arabidopsis rol1 mutants results in alterations in plant growth and cell shape formation.Plant Cell. 2008; 20: 1470-1481Crossref PubMed Scopus (74) Google Scholar) and a role of quercetin in regulating gravitropic curvature and root hair initiation (9Gayomba S.R. Muday G.K. Flavonols regulate root hair development by modulating accumulation of reactive oxygen species in the root epidermis.Development. 2020; 147dev185819Crossref PubMed Google Scholar, 11Lewis D.R. Ramirez M.V. Miller N.D. Vallabhaneni P. Ray W.K. Helm R.F. Winkel B.S.J. Muday G.K. Auxin and ethylene induce flavonol accumulation through distinct transcriptional networks.Plant Physiol. 2011; 156: 144-164Crossref PubMed Scopus (166) Google Scholar). Using mutants impaired in flavonol biosynthesis in crop species, such as tomato, has also highlighted the role of flavonol metabolites in modulating environmentally responsive signaling pathways, such as ABA-dependent guard cell signaling that induces stomatal closure (14Watkins J.M. Chapman J.M. Muday G.K. Abscisic acid-induced reactive oxygen species are modulated by flavonols to control stomata aperture.Plant Physiol. 2017; 175: 1807-1825Crossref PubMed Scopus (82) Google Scholar) and temperature-impaired pollen viability and pollen tube growth (15Muhlemann J.K. Younts T.L.B. Muday G.K. Flavonols control pollen tube growth and integrity by regulating ROS homeostasis during high-temperature stress.PNAS. 2018; 115: E11188-E11197Crossref PubMed Scopus (67) Google Scholar). Two mechanisms have been suggested to explain how flavonols regulate plant development. Flavonols function as negative regulators of auxin transport. Arabidopsis mutants with defects in flavonol synthesis have elevated levels of auxin transport (11Lewis D.R. Ramirez M.V. Miller N.D. Vallabhaneni P. Ray W.K. Helm R.F. Winkel B.S.J. Muday G.K. Auxin and ethylene induce flavonol accumulation through distinct transcriptional networks.Plant Physiol. 2011; 156: 144-164Crossref PubMed Scopus (166) Google Scholar, 16Buer C.S. Kordbacheh F. Truong T.T. Hocart C.H. Djordjevic M.A. 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. 2013; 238: 171-189Crossref PubMed Scopus (57) Google Scholar, 17Peer W.A. Bandyopadhyay A. Blakeslee J.J. Makam S.N. Chen R.J. Masson P.H. Murphy A.S. 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. 2004; 16: 1898-1911Crossref PubMed Scopus (284) Google Scholar, 18Brown D.E. Rashotte A.M. Murphy A.S. Normanly J. Tague B.W. Peer W.A. Taiz L. Muday G.K. Flavonoids act as negative regulators of auxin transport in vivo in Arabidopsis.Plant Physiol. 2001; 126: 524-535Crossref PubMed Scopus (504) Google Scholar) and flavonols block auxin transport when transport proteins are expressed in heterologous systems (19Geisler M. Blakeslee J.J. Bouchard R. Lee O.R. Vincenzetti V. Bandyopadhyay A. Titapiwatanakun B. Peer W.A. Bailly A. Richards E.L. Ejendal K.F.K. Smith A.P. Baroux C. Grossniklaus U. Müller A. et al.Cellular efflux of auxin catalyzed by the Arabidopsis MDR/PGP transporter AtPGP1.Plant J. 2005; 44: 179-194Crossref PubMed Scopus (392) Google Scholar). Second, flavonols have antioxidant capability in vitro (5Agati G. Azzarello E. Pollastri S. Tattini M. Flavonoids as antioxidants in plants: location and functional significance.Plant Sci. 2012; 196: 67-76Crossref PubMed Scopus (909) Google Scholar, 20Yonekura-Sakakibara K. Tohge T. Matsuda F. Nakabayashi R. Takayama H. Niida R. Watanabe-Takahashi A. Inoue E. Saito K. Comprehensive flavonol profiling and transcriptome coexpression analysis leading to decoding gene–metabolite correlations in Arabidopsis.Plant Cell. 2008; 20: 2160-2176Crossref PubMed Scopus (296) Google Scholar) and mutants that have impaired flavonol biosynthesis have higher levels of ROS in guard cells, root hairs, and pollen tubes (9Gayomba S.R. Muday G.K. Flavonols regulate root hair development by modulating accumulation of reactive oxygen species in the root epidermis.Development. 2020; 147dev185819Crossref PubMed Google Scholar, 10Watkins J.M. Hechler P.J. Muday G.K. Ethylene-induced flavonol accumulation in guard cells suppresses reactive oxygen species and moderates stomatal aperture.Plant Physiol. 2014; 164: 1707-1717Crossref PubMed Scopus (111) Google Scholar, 14Watkins J.M. Chapman J.M. Muday G.K. Abscisic acid-induced reactive oxygen species are modulated by flavonols to control stomata aperture.Plant Physiol. 2017; 175: 1807-1825Crossref PubMed Scopus (82) Google Scholar, 15Muhlemann J.K. Younts T.L.B. Muday G.K. Flavonols control pollen tube growth and integrity by regulating ROS homeostasis during high-temperature stress.PNAS. 2018; 115: E11188-E11197Crossref PubMed Scopus (67) Google Scholar). These two mechanisms may also be interconnected as auxin transport has been shown to be regulated by levels of ROS (21Tognetti V.B. Mühlenbock P. Breusegem F.V. Stress homeostasis – the redox and auxin perspective.Plant Cell Environ. 2012; 35: 321-333Crossref PubMed Scopus (204) Google Scholar). ROS can function as signaling molecules to regulate plant development, environmental responses, and hormone signaling (1Chapman J.M. Muhlemann J.K. Gayomba S.R. Muday G.K. RBOH-Dependent ROS synthesis and ROS scavenging by plant specialized metabolites to modulate plant development and stress responses.Chem. Res. Toxicol. 2019; 32: 370-396Crossref PubMed Scopus (50) Google Scholar, 22Nadarajah K.K. ROS homeostasis in abiotic stress tolerance in plants.Int. J. Mol. Sci. 2020; 21: 5208Crossref Scopus (23) Google Scholar, 23Kapoor D. Singh S. Kumar V. Romero R. Prasad R. Singh J. Antioxidant enzymes regulation in plants in reference to reactive oxygen species (ROS) and reactive nitrogen species (RNS).Plant Gene. 2019; 19: 100182Crossref Scopus (69) Google Scholar). The low baseline levels of ROS allow local increases in ROS to act as important developmental signals. In Arabidopsis, ROS signaling has been implicated in stomatal closure (10Watkins J.M. Hechler P.J. Muday G.K. Ethylene-induced flavonol accumulation in guard cells suppresses reactive oxygen species and moderates stomatal aperture.Plant Physiol. 2014; 164: 1707-1717Crossref PubMed Scopus (111) Google Scholar, 14Watkins J.M. Chapman J.M. Muday G.K. Abscisic acid-induced reactive oxygen species are modulated by flavonols to control stomata aperture.Plant Physiol. 2017; 175: 1807-1825Crossref PubMed Scopus (82) Google Scholar, 24Kwak J.M. Mori I.C. Pei Z.-M. Leonhardt N. Torres M.A. Dangl J.L. Bloom R.E. Bodde S. Jones J.D.G. Schroeder J.I. NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis.EMBO J. 2003; 22: 2623-2633Crossref PubMed Scopus (1167) Google Scholar, 25Okuma E. Jahan Md.S. Munemasa S. Hossain M.A. Muroyama D. Islam M.M. Ogawa K. Watanabe-Sugimoto M. Nakamura Y. Shimoishi Y. Mori I.C. Murata Y. Negative regulation of abscisic acid-induced stomatal closure by glutathione in Arabidopsis.J. Plant Physiol. 2011; 168: 2048-2055Crossref PubMed Scopus (54) Google Scholar), pollen tube growth and development (15Muhlemann J.K. Younts T.L.B. Muday G.K. Flavonols control pollen tube growth and integrity by regulating ROS homeostasis during high-temperature stress.PNAS. 2018; 115: E11188-E11197Crossref PubMed Scopus (67) Google Scholar, 26Xie H.-T. Wan Z.-Y. Li S. Zhang Y. Spatiotemporal production of reactive oxygen species by NADPH Oxidase Is critical for tapetal programmed cell death and pollen development in Arabidopsis.Plant Cell. 2014; 26: 2007-2023Crossref PubMed Scopus (125) Google Scholar, 27Potocký M. Jones M.A. Bezvoda R. Smirnoff N. Zárský V. Reactive oxygen species produced by NADPH oxidase are involved in pollen tube growth.New Phytol. 2007; 174: 742-751Crossref PubMed Scopus (289) Google Scholar, 28Kaya H. Nakajima R. Iwano M. Kanaoka M.M. Kimura S. Takeda S. Kawarazaki T. Senzaki E. Hamamura Y. Higashiyama T. Takayama S. Abe M. Kuchitsu K. Ca2+-activated reactive oxygen species production by Arabidopsis RbohH and RbohJ is essential for proper pollen tube tip growth.Plant Cell. 2014; 26: 1069-1080Crossref PubMed Scopus (154) Google Scholar), root hair elongation (9Gayomba S.R. Muday G.K. Flavonols regulate root hair development by modulating accumulation of reactive oxygen species in the root epidermis.Development. 2020; 147dev185819Crossref PubMed Google Scholar, 29Foreman Julia Demidchik V. Bothwell J.H.F. Mylona P. Miedema H. Torres M.A. Linstead P. Costa S. Brownlee C. Jones J.D.G. Davies J.M. Dolan L. Reactive oxygen species produced by NADPH oxidase regulate plant cell growth.Nature. 2003; 422: 442-446Crossref PubMed Scopus (1596) Google Scholar), root gravitropism and phototropism (30Krieger G. Shkolnik D. Miller G. Fromm H. Reactive oxygen species tune root tropic responses.Plant Physiol. 2016; 172: 1209-1220PubMed Google Scholar, 31Silva-Navas J. Moreno-Risueno M.A. Manzano C. Téllez-Robledo B. Navarro-Neila S. Carrasco V. Pollmann S. Gallego F.J. Del Pozo J.C. Flavonols mediate root phototropism and growth through regulation of proliferation-to-differentiation transition.Plant Cell. 2016; 28: 1372-1387Crossref PubMed Scopus (71) Google Scholar, 32Joo J.H. Bae Y.S. Lee J.S. Role of auxin-induced reactive oxygen species in root gravitropism.Plant Physiol. 2001; 126: 1055-1060Crossref PubMed Scopus (407) Google Scholar), primary root elongation (33Tsukagoshi H. Busch W. Benfey P.N. Transcriptional regulation of ROS controls transition from proliferation to differentiation in the root.Cell. 2010; 143: 606-616Abstract Full Text Full Text PDF PubMed Scopus (586) Google Scholar), the transition from cell proliferation to elongation in the root tip (34Mabuchi K. Maki H. Itaya T. Suzuki T. Nomoto M. Sakaoka S. Morikami A. Higashiyama T. Tada Y. Busch W. Tsukagoshi H. MYB30 links ROS signaling, root cell elongation, and plant immune responses.Proc. Natl. Acad. Sci. U. S. A. 2018; 115: E4710-E4719Crossref PubMed Scopus (35) Google Scholar), and lateral root emergence (35Orman-Ligeza B. Parizot B. de Rycke R. Fernandez A. Himschoot E. Van Breusegem F. Bennett M.J. Périlleux C. Beeckman T. Draye X. RBOH-mediated ROS production facilitates lateral root emergence in Arabidopsis.Development. 2016; 143: 3328-3339Crossref PubMed Scopus (91) Google Scholar, 36Manzano C. Pallero-Baena M. Casimiro I. Rybel B.D. Orman-Ligeza B. Isterdael G.V. Beeckman T. Draye X. Casero P. Del Pozo J.C. The emerging role of reactive oxygen species signaling during lateral root development.Plant Physiol. 2014; 165: 1105-1119Crossref PubMed Scopus (72) Google Scholar, 37Li N. Sun L. Zhang L. Song Y. Hu P. Li C. Hao F.S. AtrbohD and AtrbohF negatively regulate lateral root development by changing the localized accumulation of superoxide in primary roots of Arabidopsis.Planta. 2015; 241: 591-602Crossref PubMed Scopus (50) Google Scholar). ROS signaling is also involved in the production of the casparian strip (38Lee Y. Rubio M.C. Alassimone J. Geldner N. A mechanism for localized lignin deposition in the endodermis.Cell. 2013; 153: 402-412Abstract Full Text Full Text PDF PubMed Scopus (253) Google Scholar), and resistance to stress including hypoxia, salt stress, and ozone (39Joo J.H. Wang S. Chen J.G. Jones A.M. Fedoroff N.V. Different signaling and cell death roles of heterotrimeric G protein α and β subunits in the Arabidopsis oxidative stress response to ozone.Plant Cell. 2005; 17: 957-970Crossref PubMed Scopus (288) Google Scholar, 40Liu B. Sun L. Ma L. Hao F.-S. Both AtrbohD and AtrbohF are essential for mediating responses to oxygen deficiency in Arabidopsis.Plant Cell Rep. 2017; 36: 947-957Crossref PubMed Scopus (30) Google Scholar, 41Ma L. Zhang H. Sun L. Jiao Y. Zhang G. Miao C. Hao F. NADPH oxidase AtrbohD and AtrbohF function in ROS-dependent regulation of Na+/K+homeostasis in Arabidopsis under salt stress.J. Exp. Bot. 2012; 63: 305-317Crossref PubMed Scopus (240) Google Scholar). Yet, ROS are also produced as a result of metabolism and stress (42Foyer C.H. Noctor G. Redox homeostasis and signaling in a higher-CO2 world.Annu. Rev. Plant Biol. 2020; 71: 157-182Crossref PubMed Scopus (13) Google Scholar, 43Munné-Bosch S. Queval G. Foyer C.H. The impact of global change factors on redox signaling underpinning stress tolerance.Plant Physiol. 2013; 161: 5-19Crossref PubMed Scopus (206) Google Scholar). Therefore, plant cells have elaborate mechanisms to keep ROS at low levels to prevent oxidative damage including the production of antioxidant enzymes (42Foyer C.H. Noctor G. Redox homeostasis and signaling in a higher-CO2 world.Annu. Rev. Plant Biol. 2020; 71: 157-182Crossref PubMed Scopus (13) Google Scholar, 44Mhamdi A. Queval G. Chaouch S. Vanderauwera S. Van Breusegem F. Noctor G. Catalase function in plants: a focus on Arabidopsis mutants as stress-mimic models.J. Exp. Bot. 2010; 61: 4197-4220Crossref PubMed Scopus (471) Google Scholar, 45Passaia G. Margis-Pinheiro M. Glutathione peroxidases as redox sensor proteins in plant cells.Plant Sci. 2015; 234: 22-26Crossref PubMed Scopus (53) Google Scholar) and specialized metabolites, such as flavonols (1Chapman J.M. Muhlemann J.K. Gayomba S.R. Muday G.K. RBOH-Dependent ROS synthesis and ROS scavenging by plant specialized metabolites to modulate plant development and stress responses.Chem. Res. Toxicol. 2019; 32: 370-396Crossref PubMed Scopus (50) Google Scholar). Flavonoids have been implicated in controlling root development (9Gayomba S.R. Muday G.K. Flavonols regulate root hair development by modulating accumulation of reactive oxygen species in the root epidermis.Development. 2020; 147dev185819Crossref PubMed Google Scholar, 18Brown D.E. Rashotte A.M. Murphy A.S. Normanly J. Tague B.W. Peer W.A. Taiz L. Muday G.K. Flavonoids act as negative regulators of auxin transport in vivo in Arabidopsis.Plant Physiol. 2001; 126: 524-535Crossref PubMed Scopus (504) Google Scholar, 19Geisler M. Blakeslee J.J. Bouchard R. Lee O.R. Vincenzetti V. Bandyopadhyay A. Titapiwatanakun B. Peer W.A. Bailly A. Richards E.L. Ejendal K.F.K. Smith A.P. Baroux C. Grossniklaus U. Müller A. et al.Cellular efflux of auxin catalyzed by the Arabidopsis MDR/PGP transporter AtPGP1.Plant J. 2005; 44: 179-194Crossref PubMed Scopus (392) Google Scholar, 46Maloney G.S. DiNapoli K.T. Muday G.K. The anthocyanin reduced tomato mutant demonstrates the role of flavonols in tomato lateral root and root hair development.Plant Physiol. 2014; 166: 614-631Crossref PubMed Scopus (59) Google Scholar), yet whether specific flavonols control distinct aspects of root development has not been fully tested. The primary root forms within the embryo and emerges from the seedling. Lateral roots form post embryonically to increase root branching for stability and to maximize nutrient and water uptake (47Lynch J. Root architecture and plant productivity.Plant Physiol. 1995; 109: 7-13Crossref PubMed Scopus (1137) Google Scholar, 48Lynch J.P. Rightsizing root phenotypes for drought resistance.J. Exp. Bot. 2018; 69: 3279-3292Crossref PubMed Scopus (57) Google Scholar). The primary and lateral roots are then covered with small single cell projections called root hairs that maximize the surface area of roots (49Grierson C. Nielsen E. Ketelaarc T. Schiefelbein J. Root hairs.Arabidopsis Book. 2014; 12e0172Crossref PubMed Google Scholar). Lateral roots initiate from founder cells in the pericycle that remained competent to divide during their transition from the root apical meristem to the differentiation zone of the root (50Malamy J.E. Benfey P.N. Organization and cell differentiation in lateral roots of Arabidopsis thaliana.Development. 1997; 124: 33-44Crossref PubMed Google Scholar). After founder cells begin to divide asymmetrically, the lateral root primordium (LRP) develops through a series of eight stages (50Malamy J.E. Benfey P.N. Organization and cell differentiation in lateral roots of Arabidopsis thaliana.Development. 1997; 124: 33-44Crossref PubMed Google Scholar, 51Santos Teixeira J.A. ten Tusscher K.H. The systems biology of lateral root formation: connecting the dots.Mol. Plant. 2019; 12: 784-803Abstract Full Text Full Text PDF PubMed Scopus (15) Google Scholar, 52Du Y. Scheres B. Lateral root formation and the multiple roles of auxin.J. Exp. Bot. 2018; 69: 155-167Crossref PubMed Scopus (119) Google Scholar) where the LRP expands through the endodermis, cortex, and finally emerges through the epidermis. This process is regulated by mechanical signals (53Swarup K. Benková E. Swarup R. Casimiro I. Péret B. Yang Y. Parry G. Nielsen E. De Smet I. Vanneste S. Levesque M.P. Carrier D. James N. Calvo V. Ljung K. et al.The auxin influx carrier LAX3 promotes lateral root emergence.Nat. Cell Biol. 2008; 10: 946-954Crossref PubMed Scopus (516) Google Scholar, 54Ditengou F.A. Teale W.D. Kochersperger P. Flittner K.A. Kneuper I. van der Graaff E. Nziengui H. Pinosa F. Li X. Nitschke R. Laux T. Palme K. Mechanical induction of lateral root initiation in Arabidopsis thaliana.PNAS. 2008; 105: 18818-18823Crossref PubMed Scopus (199) Google Scholar, 55Richter G.L. Monshausen G.B. Krol A. Gilroy S. Mechanical stimuli modulate lateral root organogenesis.Plant Physiol. 2009; 151: 1855-1866Crossref PubMed Scopus (111) Google Scholar, 56Laskowski M. Grieneisen V.A. Hofhuis H. Hove C.A.T. Hogeweg P. Marée A.F.M. Scheres B. Root system architecture from coupling cell shape to auxin transport.PLoS Biol. 2008; 6: e307Crossref PubMed Scopus (290) Google Scholar), hormonal signals including auxin (53Swarup K. Benková E. Swarup R. Casimiro I. Péret B. Yang Y. Parry G. Nielsen E. De Smet I. Vanneste S. Levesque M.P. Carrier D. James N. Calvo V. Ljung K. et al.The auxin influx carrier LAX3 promotes lateral root emergence.Nat. Cell Biol. 2008; 10: 946-954Crossref PubMed Scopus (516) Google Scholar), and biochemical signals such as ROS or nitric oxide (57Méndez-Bravo A. Raya-González J. Herrera-Estrella L. López-Bucio J. Nitric Oxide is involved in alkamide-induced lateral root development in Arabidopsis.Plant Cell Physiol. 2010; 51: 1612-1626Crossref PubMed Scopus (54) Google Scholar). Flavonoids have been suggested to regulate lateral root development, based on an increased number of lateral roots in plants with mutations in the gene encoding the first committed step of flavonoid biosynthesis catalyzed by chalcone synthase. Although both tt4(2YY6) (18Brown D.E. Rashotte A.M. Murphy A.S. Normanly J. Tague B.W. Peer W.A. Taiz L. Muday G.K. Flavonoids act as negative regulators of auxin transport in vivo in Arabidopsis.Plant Physiol. 2001; 126: 524-535Crossref PubMed Scopus (504) Google Scholar) and tt4-1 (58Buer C.S. Djordjevic M.A. Architectural phenotypes in the transparent testa mutants of Arabidopsis thaliana.J. Exp. Bot. 2009; 60: 751-763Crossref PubMed Scopus (90) Google Scholar) mutants form more lateral roots than wild-type, the specific flavonoids that modulate this process have not been examined, and it is not clear whether this function is through flavonoid antioxidant activity. This contrasts with root hairs, whose synthesis is also repressed by flavonols, with a specific role for one flavonol, quercetin in controlling root hair formation via modulating ROS levels (9Gayomba S.R. Muday G.K. Flavonols regulate root hair development by modulating accumulation of reactive oxygen species in the root epidermis.Development. 2020; 147dev185819Crossref PubMed Google Scholar). This study examined the role of flavonols in modulating lateral root development and tested the hypothesis that flavonoids regulate this developmental process by scavenging ROS within the LRP. We quantified primordia and emerged lateral roots in a suite of flavonoid biosynthetic mutants, revealing that mutants that produce no flavonols had increased lateral root emergence. In contrast, a mutant that produces kaempferol at higher than wild-type levels and produces no other flavonols had fewer emerged lateral roots than wild-type, suggesting that kaempferol or downstream derivatives of this flavonol negatively regulate lateral root emergence. Consistent with an inhibitory effect of kaempferol, there is a negative correlation between the amount of kaempferol and the number of emerged lateral roots across multiple mutant lines. Using confocal microscopy and dyes that fluoresce upon binding flavonols or in response to oxidation by ROS, we find that in regions of roots with high levels of flavonols, there is decreased ROS abundance and in areas of high ROS, there are low concentrations of flavonols. These experiments support the model that flavonol-modulated root development is orchestrated by the scavenging of ROS within the lateral root primordia. The flavonoid biosynthetic pathway is well characterized in Arabidopsis, with mutations mapped to the genes encoding each biosynthetic enzyme. The flavonoid biosynthetic pathway and the enzymes defective in these mutants are shown in Figure 1. We verified the metabolite profiles in the roots of the mutant alleles used in this study and under our specific growth conditions using liquid chromatography–mass spectroscopy (LC-MS). Flavonols underwent acid hydrolysis to remove any glycosylation prior to MS1 analysis to determine their concentration with standard curves and the aglycone flavonols were verified by MS2 (Table S1). Flavonol levels were quantified in Col-0 and six mutants with defects in genes encoding enzymes involved in flavonoid biosynthesis. The flavonol" @default.
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• W3115804594 creator A5022648068 @default.
• W3115804594 creator A5066895150 @default.
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• W3115804594 title "Flavonols modulate lateral root emergence by scavenging reactive oxygen species in Arabidopsis thaliana" @default.
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• W3115804594 doi "https://doi.org/10.1074/jbc.ra120.014543" @default.
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