MeJA Affects Root Growth by Modulation of Transmembrane Auxin Flux in the Transition Zone

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• 作者：Suli Yan ; Ting Zhang ; Shanshan Dong…
• 关键词：Auxin flux ; H+ flux ; Jasmonate ; COI1 ; Arabidopsis thaliana
• 刊名：Journal of Plant Growth Regulation
• 出版年：2016
• 出版时间：March 2016
• 年：2016
• 卷：35
• 期：1
• 页码：256-265
• 全文大小：4,092 KB
• 参考文献：Baluska F, Mancuso S, Volkmann D, Barlow PW (2010) Root apex transition zone: a signalling-response nexus in the root. Trends Plant Sci 15:402–408CrossRef PubMed
  Blilou I, Xu J, Wildwater M, Willemsen V, Paponov I, Friml J, Heidstra R, Aida M, Palme K, Scheres B (2005) The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 433:39–44CrossRef PubMed
  Chen Q, Sun J, Zhai Q, Zhou W, Qi L, Xu L, Wang B, Chen R, Jiang H, Qi J, Li X, Palme K, Li C (2011) The basic Helix-Loop-Helix transcription factor MYC2 directly represses PLETHORA expression during Jasmonate-mediated modulation of the root stem cell niche in Arabidopsis. Plant Cell 23:3335–3352PubMedCentral CrossRef PubMed
  Chini A, Fonseca S, Fernández G, Adie B, Chico JM, Lorenzo O, Garcia-Casado G, López-Vidriero I, Lozano FM, Ponce MR, Micol JL, Solano R (2007) The JAZ family of repressors is the missing link in jasmonate signalling. Nature 448:666–671CrossRef PubMed
  Cho D, Villiers F, Kroniewicz L, Lee S, Seo YJ, Hirschi KD, Leonhardt N, Kwak JM (2012) Vacuolar CAX1 and CAX3 influence auxin transport in guard cells via regulation of apoplastic pH. Plant Physiol 160:1293–1302PubMedCentral CrossRef PubMed
  Coley PD, Bryant JP, Chapin FS (1985) Resource availability and plant anti herbivore defense. Science 23:895–900CrossRef
  Creelman RA, Mullet JE (1997) Oligosaccharins, brassinolides, and jasmonates: Nontraditional regulators of plant growth, development, and gene expression. Plant Cell 9:1211–1223PubMedCentral CrossRef PubMed
  Dathe W, Rönsch H, Preiss A, Schade W, Sembdner G, Schreiber K (1981) Endogenous plant hormones of the broad bean, Vicia faba L. (-)-jasmonic acid, a plant growth inhibitor in pericarp. Planta 153:530–535CrossRef PubMed
  Delbarre A, Müller P, Imhoff V, Guern J (1996) Comparison of mechanisms controlling uptake and accumulation of 2,4-dichlorophenoxy acetic acid, naphthalene-1-acetic acid, and indole-3-acetic acid in suspension-cultured tobacco cells. Planta 198:833–844CrossRef
  Feys B, Benedetti CE, Penfold CN, Turner JG (1994) Arabidopsis mutants selected for resistance to the phytotoxin coronatine are male sterile, insensitive to methyl jasmonate, and resistant to a bacterial pathogen. Plant Cell 6:751–759PubMedCentral CrossRef PubMed
  Goldsmith MHM (1982) A saturable site responsible for polar transport of indole-3-acetic acid in sections of maize coleoptiles. Planta 155:68–75CrossRef PubMed
  Grieneisen VA, Xu J, Marée AF, Hogeweg P, Scheres B (2007) Auxin transport is sufficient to generate a maximum and gradient guiding root growth. Nature 449:1008–1013CrossRef PubMed
  Haruta M, Sussman MR (2012) The effect of a genetically reduced plasma membrane proton motive force on vegetative growth of Arabidopsis. Plant Physiol 158:1158–1171PubMedCentral CrossRef PubMed
  Hentrich M, Böttcher C, Düchting P, Cheng Y, Zhao Y, Berkowitz O, Masle J, Medina J, Pollmann S (2013) The jasmonic acid signaling pathway is linked to auxin homeostasis through the modulation of YUCCA8 and YUCCA9 gene expression. Plant J 74:626–637PubMedCentral CrossRef PubMed
  Li L, Li C, Lee GI, Howe GA (2002) Distinct roles for jasmonate synthesis and action in the systemic wound response of tomato. Proc Natl Acad Sci 99:6416–6421PubMedCentral CrossRef PubMed
  Mancuso S, Marras AM, Magnus V, Baluska F (2005) Noninvasive and continuous recordings of auxin fluxes in intact root apex with a carbon nanotube-modified and self-referencing microelectrode. Anal Biochem 341:344–351CrossRef PubMed
  McConn M, Browse J (1996) The critical requirement for linolenic acid is pollen development, not photosynthesis, in an Arabidopsis mutant. Plant Cell 8:403–416PubMedCentral CrossRef PubMed
  McLamore ES, Diggs A, Calvo Marzal P, Shi J, Blakeslee JJ, Peer WA, Murphy AS, Porterfield DM (2010) Non-invasive quantification of endogenous root auxin transport using an integrated flux microsensor technique. Plant J 63:1004–1016CrossRef PubMed
  Morisawa MS, Steinhardt RA (1982) Changes in intracellular pH of Physarum plasmodium during the cell cycle and in response to starvation. Exp Cell Res 140:341–352CrossRef PubMed
  Pan X, Welti R, Wang X (2010) Quantitative analysis of major plant hormones in crude plant extracts by high-performance liquid chromatography–mass spectrometry. Nat Protoc 5:986–992CrossRef PubMed
  Petersson SV, Johansson AI, Kowalczyk M, Makoveychuk A, Wang JY, Moritz T, Grebe M, Benfey PN, Sandberg G, Ljung K (2009) An auxin gradient and maximum in the Arabidopsis root apex shown by high-resolution cell-specific analysis of IAA distribution and synthesis. Plant Cell 21:1659–1668PubMedCentral CrossRef PubMed
  Porterfield DM, McLamore ES, Banks MK (2009) Microsensor technology for measuring H+ flux in buffered media. Sens Actuator B 136:383–387CrossRef
  Qi L, Yan J, Li Y, Jiang H, Sun J, Chen Q, Li H, Chu J, Yan C, Sun X, Yu Y, Li C, Li C (2012) Arabidopsis thaliana plants differentially modulate auxin biosynthesis and transport during defense responses to the necrotrophic pathogen Alternaria brassicicola. New Phytol 195:872–882CrossRef PubMed
  Rahman A, Bannigan A, Sulaman W, Pechter P, Blancaflor EB, Baskin TI (2007) Auxin, actin and growth of the Arabidopsis thaliana primary root. Plant J 50:514–528CrossRef PubMed
  Rober-Kleber N, Albrechtova JT, Fleig S, Huck N, Michalke W, Wagner E, Speth V, Neuhaus G, Fischer-Iglesias C (2003) Plasma membrane H+-ATPase is involved in auxin-mediated cell elongation during wheat embryo development. Plant Physiol 131:1302–1312PubMedCentral CrossRef PubMed
  Rubery PH, Sheldrake AR (1974) Carrier-mediated auxin transport. Planta 118:101–121CrossRef PubMed
  Schommer C, Palatnik JF, Aggarwal P, Chételat A, Cubas P, Farmer EE, Nath U, Weigel D (2008) Control of jasmonate biosynthesis and senescence by miR319 targets. PLoS Biol 6:1991–2001CrossRef
  Sheard LB, Tan X, Mao H, Withers J, Ben-Nissan G, Hinds TR, Kobayashi Y, Hsu FF, Sharon M, Browse J, He SY, Rizo J, Howe GA, Zheng N (2010) Jasmonate perception by inositol-phosphate-potentiated COI1-JAZ co-receptor. Nature 468:400–405PubMedCentral CrossRef PubMed
  Song SS, Qi TC, Fan M, Zhang X, Gao H, Huang H, Wu DW, Guo HW, Xie DX (2013) The bHLH subgroup IIId factors negatively regulate jasmonate-mediated plant defense and development. PLoS Genet 9:e1003653PubMedCentral CrossRef PubMed
  Staswick PE, Su W, Howell SH (2009) Methyl jasmonate inhibition of root growth and induction of a leaf protein are decreased in an Arabidopsis thaliana mutant. Proc Natl Acad Sci 89:6837–6840CrossRef
  Stepanova AN, Robertson-Hoyt J, Yun J, Benavente LM, Xie DY, Dolezal K, Schlereth A, Jürgens G, Alonso JM (2008) TAA1-mediated auxin biosynthesis is essential for hormone crosstalk and plant development. Cell 133:177–191CrossRef PubMed
  Subraya KK, Diggs A, Porterfield DM (2013) Amperometric biosensor approaches for quantification of indole 3-acetic acid in plant stress responses. Commun Soil Sci Plan 44:1749–1763CrossRef
  Sun J, Xu Y, Ye S, Jiang H, Chen Q, Liu F, Zhou W, Chen R, Li X, Tietz O, Wu X, Cohen JD, Palme K, Li C (2009) Arabidopsis ASA1 is important for jasmonate-mediated regulation of auxin biosynthesis and transport during lateral root formation. Plant Cell 21:1495–1511PubMedCentral CrossRef PubMed
  Sun J, Chen Q, Qi L, Jiang H, Li S, Xu Y, Liu F, ZhouW Pan J, Li X, Palme K, Li C (2011) Jasmonate modulates endocytosis and plasma membrane accumulation of the Arabidopsis PIN2 protein. New Phytol 191:360–375CrossRef PubMed
  Sussman MR, Goldsmith MH (1981) The action of specific inhibitors of auxin transport on uptake of auxin and binding of N-1-naphthylphthalamic acid to a membrane site in maize coleoptiles. Planta 152:13–18CrossRef PubMed
  Taiz L, Zeiger E (2006) Plant physiology, 4th edn. Sinauer Associates, US, Sunderland
  Thines B, Katsir L, Melotto M, Niu Y, Mandaokar A, Liu G, Nomura K, He SY, Howe GA, Browse J (2007) JAZ repressor proteins are targets of the SCF(COI1) complex during jasmonate signalling. Nature 448:661–665CrossRef PubMed
  Turner JG, Ellis C, Devoto A (2002) The jasmonate signal pathway. Plant Cell 14:S153–S164PubMedCentral PubMed
  Ulmasov T, Murfett J, Hagen G, Guilfoyle TJ (1997) Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell 9:1963–1971PubMedCentral CrossRef PubMed
  Undurraga SF, Santos MP, Paez-Valencia J, Yang H, Hepler PK, Facanha AR, Hirschi KD, Gaxiola RA (2012) Arabidopsis sodium dependent and independent phenotypes triggered by H+-PPase up-regulation are SOS1 dependent. Plant Sci 183:96–105CrossRef PubMed
  Vanneste S, Friml J (2009) Auxin: a trigger for change in plant development. Cell 136:1005–1016CrossRef PubMed
  Wasternack C, Kombrink E (2010) Jasmonates: structural requirements for lipid-derived signals active in plant stress responses and development. ACS Chem Biol 5:55–77CrossRef
  Wen B, Bin J, Wang X (2006) Effects of methyl jasmonate and abscisic acid treatments on the hydrolysis activity of plasma membrane H+-ATPase in Mung Bean (Vigna radiata L). Plant Physiol J 42:855–859
  Wisniewska J, Xu J, Seifertova D, Brewer PB, Ruzicka K, Blilou I, Rouquie D, Benkova E, Scheres B, Friml J (2006) Polar PIN localization directs auxin flow in plants. Science 312:883CrossRef PubMed
  Wolters H, Jürgens G (2009) Survival of the flexible: Hormonal growth control and adaptation in plant development. Nat Rev Genet 10:305–317CrossRef PubMed
  Xie DX, Feys BF, James S, Nieto-Rostro M, Turner JG (1998) COI1: an Arabidopsis gene required for jasmonate-regulated defense and fertility. Science 280:1091–1094CrossRef PubMed
  Xu Y, Sun T, Yin L (2006) Application of non-invasive microsensing system to simultaneously measure both H+ and O2 fluxes around the pollen tube. J Integr Plant Biol 48:823–832CrossRef
  Xu W, Jia L, Baluška F, Ding G, Shi W, Ye N, Zhang J (2012) PIN2 is required for the adaptation of Arabidopsis roots to alkaline stressby modulating proton secretion. J Exp Bot 63:6105–6114PubMedCentral CrossRef PubMed
  Xu W, Jia L, Shi W, Liang J, Zhou F, Li Q, Zhang J (2013) Abscisic acid accumulation modulates auxin transport in the root tip to enhance proton secretion for maintaining root growth under moderate water stress. New Phytol 197:139–150CrossRef PubMed
  Yan J, Zhang C, Gu M, Bai Z, Zhang W, Qi T, Cheng Z, Peng W, Luo H, Nan F, Wang Z, Xie D (2009) The Arabidopsis CORONATINE INSENSITIVE1 protein is a jasmonate receptor. Plant Cell 21:2220–2236PubMedCentral CrossRef PubMed
  Yan SL, Luo ST, Dong SS, Zhang T, Sun JR, Wang NN, Yao HJ, Shen YB (2015) Heterotrimeric G-proteins involved in the MeJA regulated ion flux and stomatal closure in Arabidopsis thaliana. Funct Plant Biol 42:126–135CrossRef
  Yang Y, Hammes UZ, Taylor CG, Schachtman DP, Nielsen E (2006) High-affinity auxin transport by the AUX1 influx carrier protein. Curr Biol 16:1123–1127CrossRef PubMed
  Yang ZB, Geng X, He C, Zhang F, Wang R, Horst WJ, Ding Z (2014) TAA1-regulated local auxin biosynthesis in the root-apex transition zone mediates the aluminum-induced inhibition of root growth in Arabidopsis. Plant Cell 26:2889–2904PubMedCentral CrossRef PubMed
  Zhang Y, Turner JG (2008) Wound-induced endogenous jasmonates stunt plant growth by inhibiting mitosis. PLoS One 3:e3699PubMedCentral CrossRef PubMed
  Zhao Y, Hull AK, Gupta NR, Goss KA, Alonso J, Ecker JR, Normanly J, Chory J, Celenza JL (2002) Trp-dependent auxin biosynthesis in Arabidopsis: involvement of cytochrome P450s CYP79B2 and CYP79B3. Genes Dev 16:3100–3112PubMedCentral CrossRef PubMed
  
• 作者单位：Suli Yan (1) (2)
  Ting Zhang (1) (2)
  Shanshan Dong (1) (2)
  Eric Scott McLamore (3)
  Ningning Wang (1) (2)
  Xiaoyi Shan (1)
  Yingbai Shen (1) (2)
  Yinglang Wan (1)
  
  1. College of Biological Sciences and Technology, Beijing Forestry University, Beijing, 100083, China
  2. National Engineering Laboratory for Tree Breeding, Beijing Forestry University, Beijing, 100083, China
  3. Agricultural and Biological Engineering Department, University of Florida, Gainesville, FL, 32611, USA
  
• 刊物类别：Biomedical and Life Sciences
• 刊物主题：Life Sciences
  Plant Sciences
  Cell Biology
  Agriculture
  Forestry
  
• 出版者：Springer New York
• ISSN：1435-8107

文摘

Biosynthesis and accumulation of jasmonate (JA) can regulate plant defense responses and organ development under insect herbivore stress conditions. One of these responses, the inhibition of root growth, is a common phenomenon. However, the physiological and molecular mechanisms of how JA affects root growth are not completely understood. In this study, the influence of MeJA treatment on auxin and proton flux rates in the root apex region of Col-0, coi1-1, pin2, and aux1-7 mutant lines was examined using a non-invasive micro-test technique. The auxin and H+ flux profiles taken from coi1-1 mutants suggest that the modulation of auxin and H+ flux by JA requires the function of COI1. The auxin and H+ flux in pin2 and aux1 mutants with and without JA treatment suggest that JA can affect polar auxin transport by regulating PIN-mediated auxin efflux and the AUX-mediated influx pathways. Furthermore, the expression levels of PIN1, PIN2, PIN3, PIN7, AUX1, and TIR1 genes were reduced under MeJA treatment, and expression levels of CYP79B2 and CYP79B3 were elevated. Together, these results suggest that JA signaling may modulate the auxin signaling pathways by regulating the expression of key genes.