DOI QR코드

DOI QR Code

Recent research progress on acid-growth theory

산-생장설에 대한 최근 연구 동향

  • Lee, Sang Ho (Division of Biomedical Engineering and Health Management Sciences, Mokwon University)
  • 이상호 (목원대학교 의생명.보건학부)
  • Received : 2016.12.06
  • Accepted : 2016.12.21
  • Published : 2016.12.31

Abstract

Auxins are essential in plant growth and development. The auxin-stimulated elongation of plant cells has been explained by the "acid-growth theory", which was proposed forty years ago. According to this theory, the auxin activates plasma membrane $H^+-ATPase$ to induce proton extrusion into the apoplast, promoting cell expansion through the activation of cell wall-loosening proteins such as expansins. Even though accepted as the classical theory of auxin-induced cell growth for decades, the major signaling components comprising this model were unknown, until publication of recent reports. The major gap in the acid growth theory is the signaling mechanism by which auxin activates the plasma membrane $H^+-ATPase$. Recent genetic, molecular, and biochemical approaches reveal that several auxin-related molecules, such as TIR1/AFB AUX/IAA coreceptors and SMALL AUXIN UP RNA (SAUR), serve as important components of the acid-growth model, phosphorylating and subsequently activating the plasma membrane $H^+-ATPase$. These researches reestablish the four-decade-old theory by providing us the detailed signaling mechanism of auxininduced cell growth. In this review, we discuss the recent research progress in auxin-induced cell elongation, and a set of possible future works based on the reestablished acid-growth model.

Keywords

References

  1. Badescu GO, Napier RM (2006) Receptors for auxin: will it all end in TIRs? Trends Plant Sci 11:217-223 https://doi.org/10.1016/j.tplants.2006.03.001
  2. Baxter I, Tchieu J, Sussman MR, Boutry M, Palmgren MG, Gribskov M, Harper JF, Axelsen KB (2003) Genomic comparison of P-type ATPase ion pumps in Arabidopsis and rice. Plant Physiol 132:618-628 https://doi.org/10.1104/pp.103.021923
  3. Chae K, Isaacs CG, Reeves PH, Maloney GS, Muday GK, Nagpal P, Reed JW (2012) Arabidopsis SMALL AUXIN UP RNA63 promotes hypocotyl and stamen filament elongation. Plant J 71:684-697 https://doi.org/10.1111/j.1365-313X.2012.05024.x
  4. Chen Y, Hoehenwarter W, Weckwerth W (2010) Comparative analysis of phytohormone-responsive phosphoproteins in Arabidopsis thaliana using $TiO_2$-phosphopeptide enrichment and mass accuracy precursor alignment. Plant J 63:1-17
  5. Cho M, Lee OR, Ganguly A, Cho H-T (2007) Auxin signaling: short and long. J Plant Biol 50:79-89 https://doi.org/10.1007/BF03030615
  6. Claussen M, Luthen H, Blatt M, Bottger M (1997) Auxin-induced growth and its linkage to potassium channels. Planta 201:227-234 https://doi.org/10.1007/BF01007708
  7. Darwin C (1880) The Power of Movement in Plants. John Murray, London, UK, 468-477
  8. Dharmasiri N, Dharmasiri S, Estelle M (2005) The F-box protein TIR1 is an auxin receptor. Nature 435:441-445 https://doi.org/10.1038/nature03543
  9. Duby G, Boutry M (2009) The plant plasma membrane proton pump ATPase: a highly regulated P-type ATPase with multiple physiological roles. Pflugers Arch 457:645-655 https://doi.org/10.1007/s00424-008-0457-x
  10. Enders TA, Strader LC (2014) Auxin activity: past, present, and future. Am J Bot 102:180-196
  11. Fendrych M, Leung J, Friml J (2016) TIR1/AFB-Aux/IAA auxin perception mediates rapid cell wall acidification and growth of Arabidopsis hypocotyls. eLife 5:e19048
  12. Franklin KA, Lee SH, Patel D, Kumar SV, Spartz AK, Gu C, Ye S, Yu P, Breen G, Cohen JD, Wigge PA, Gray WM (2011) PHYTOCHROME-INTERACTING FACTOR 4 (PIF4) regulates auxin biosynthesis at high temperature. Proc Natl Acad Sci USA 108:20231-20235 https://doi.org/10.1073/pnas.1110682108
  13. Fuglsang AT, Visconti S, Drumm K, Jahn T, Stensballe A, Mattei B, Jensen ON, Aducci P, Palmgren MG (1999) Binding of 14-3-3 protein to the plasma membrane $H^{(+)}$-ATPase AHA2 involves the three C-terminal residues $Tyr^{(946)}$-Thr-Val and requires phosphorylation of $Thr^{(947)}$. J Biol Chem 274:36774-36780 https://doi.org/10.1074/jbc.274.51.36774
  14. Gao Y, Zhang Y, Zhang D, Dai X, Estelle M, Zhao Y (2015) Auxin binding protein 1 (ABP1) is not required for either auxin signaling or Arabidopsis development. Proc Natl Acad Sci USA 112:2275-2280 https://doi.org/10.1073/pnas.1500365112
  15. Hagen G, Guilfoyle T (2002) Auxin-responsive gene expression: genes, promoters and regulatory factors. Plant Mol Biol 49:373-385 https://doi.org/10.1023/A:1015207114117
  16. Hager A (2003) Role of the plasma membrane $H^+$-ATPase in auxin-induced elongation growth: historical and new aspects. J Plant Res 116:483-505 https://doi.org/10.1007/s10265-003-0110-x
  17. Hager A, Menzel H, Krauss A (1971) Versuche und Hypothese zur Primarwirkung des Auxins beim Streckungswachtum. Planta 100:47-75 https://doi.org/10.1007/BF00386886
  18. Haruta M, Burch HL, Nelson RB, Barrett-Wilt G, Kline KG, Mohsin SB, Young JC, Otegui MS, Sussman MR (2010) Molecular characterization of mutant Arabidopsis plants with reduced plasma membrane proton pump activity. J Biol Chem 285:17918-17929 https://doi.org/10.1074/jbc.M110.101733
  19. Hedrich R, Moran O, Conti F, Busch H, Becker D, Gambale F, Dreyer I, Kuch A, Neuwinger K, Palme K (1995) Inward rectifier potassium channels in plants differ from their animal counterparts in response to voltage and channel modulators. Eur Biophys J 124:107-115
  20. Jelich-Ottmann C, Weiler EW, Oecking C (2001) Binding of regulatory 14-3-3 proteins to the C terminus of the plant plasma membrane $H^+$-ATPpase involves part of its autoinhibitory region. J Biol Chem 276:39852-39857 https://doi.org/10.1074/jbc.M106746200
  21. Kepinski S, Leyser O (2005) The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature 435:446-451 https://doi.org/10.1038/nature03542
  22. Kerkeb L, Venema K, Donaire JP, Rodriguez-Rosales MP (2002) Enhanced $H^+$/ATP coupling ratio of $H^+$-ATPase and increased 14-3-3 protein content in plasma membrane of tomato cells upon osmotic shock. Physiol Plant 116:37-41 https://doi.org/10.1034/j.1399-3054.2002.1160105.x
  23. Kinoshita T, Shimazaki K (1999) Blue light activates the plasma membrane $H^+$-ATPase by phosphorylation of the C-terminus in stomatal guard cells. EMBO J 18:5548-5558 https://doi.org/10.1093/emboj/18.20.5548
  24. Knox K, Grierson CS, Leyser O (2003) AXR3 and SHY2 interact to regulate root hair development. Development 130:5769-5777 https://doi.org/10.1242/dev.00659
  25. Kong Y, Zhu Y, Gao C, She W, Lin W, Chen Y, Han N, Bian H, Zhu M, Wang J (2013) Tissue-specific expression of SMALL AUXIN UP RNA41 differentially regulates cell expansion and root meristem patterning in Arabidopsis. Plant Cell Physiol 54:609-621 https://doi.org/10.1093/pcp/pct028
  26. Lee SH (2013) Auxin-responsive SMALL AUXIN UP RNA genes: recent research progress and its application for crop improvement. J Plant Biotechnol 40:59-64 https://doi.org/10.5010/JPB.2013.40.2.059
  27. Leyser O (2006) Dynamic integration of auxin transport and signaling. Curr Biol 16:R424-R433 https://doi.org/10.1016/j.cub.2006.05.014
  28. Leyser HM, Pickett FB, Dharmasiri S, Estelle M (1996) Mutations in the AXR3 gene of Arabidopsis result in altered auxin response including ectopic expression from the SAUR-AC1 promoter. Plant J 10:403-413 https://doi.org/10.1046/j.1365-313x.1996.10030403.x
  29. Lobler M, Klambt D (1985) Auxin-binding protein from coleoptile membranes of corn (Zea mays L.). J Biol Chem 260:9854-9859
  30. Michalko J, Dravecka M, Bollenbach T, Friml J (2015) Embryo-lethal phenotypes in early abp1 mutants are due to disruption of the neighboring BSM gene. F1000Res 4:e19048
  31. Morsomme P, Boutry M (2000) The plant plasma membrane $H^+$-ATPase: structure, function and regulation. Biochim Biophys Acta 1465:1-16 https://doi.org/10.1016/S0005-2736(00)00128-0
  32. Napier RM, David KM, Perrot-Rechenmann CA (2002) Short history of auxin-binding proteins. Plant Mol Biol 49:339-348 https://doi.org/10.1023/A:1015259130955
  33. Niittyla T, Fuglsang AT, Palmgren MG, Frommer WB, Schulze WX (2007) Temporal analysis of sucrose-induced phosphorylation changes in plasma membrane proteins of Arabidopsis. Mol Cell Proteomics 6: 1711-1726 https://doi.org/10.1074/mcp.M700164-MCP200
  34. Palmgren MG (2001) Plant plasma membrane $H^+$-ATPases: powerhouses for nutrient uptake. Annu Rev Plant Physiol Plant Mol Biol 52:817-845 https://doi.org/10.1146/annurev.arplant.52.1.817
  35. Park JE, Kim YS, Yoon HK, Park CM (2007) Functional characterization of a small auxin-up RNA gene in apical hook development in Arabidopsis. Plant Sci 172:150-157 https://doi.org/10.1016/j.plantsci.2006.08.005
  36. Quint M, Gray WM (2006) Auxin signaling. Curr Opin Plant Biol 9:448-453 https://doi.org/10.1016/j.pbi.2006.07.006
  37. Rayle DL, Cleland R (1970) Enhancement of wall loosening and elongation by acid solutions. Plant Physiol 46:250-253 https://doi.org/10.1104/pp.46.2.250
  38. Ren H, Gray WM (2015) SAUR proteins as effectors of hormonal and environmental signals in plant growth. Mol Plant 8:1-12 https://doi.org/10.1016/j.molp.2014.12.009
  39. Schenck D, Christian M, Jones A, Luthen H (2010) Rapid auxin-induced cell expansion and gene expression: a four-decade-old question revisited. Plant Physiol 152:1183-1185 https://doi.org/10.1104/pp.109.149591
  40. Spartz AK, Lee SH, Wenger JP, Gonzalez N, Itoh H, Inze D, Peer WA, Murphy AS, Overvoorde P, Gray WM (2012) The SAUR19 subfamily of SMALL AUXIN UP RNA genes promote cell expansion. Plant J 70:978-990 https://doi.org/10.1111/j.1365-313X.2012.04946.x
  41. Spartz AK, Ren H, Park MY, Grandt KN, Lee SH, Murphy AS, Sussman MR, Overvoorde PJ, Gray WM (2014) SAUR inhibition of PP2C-D phosphatases activates plasma membrane $H^+$-ATPases to promote cell expansion in Arabidopsis. Plant Cell 26:2129-2142 https://doi.org/10.1105/tpc.114.126037
  42. Stamm P, Kumar PP (2013) Auxin and gibberellin responsive Arabidopsis SMALL AUXIN UP RNA36 regulates hypocotyl elongation in the light. Plant Cell Rep 32:759-769 https://doi.org/10.1007/s00299-013-1406-5
  43. Takahashi K, Hayashi K, Kinoshita T (2012) Auxin activates the plasma membrane $H^+$-ATPase by phosphorylation during hypocotyl elongation in Arabidopsis. Plant Physiol 159:632-641 https://doi.org/10.1104/pp.112.196428
  44. Thimann KV, Bonner J (1932) Studies on the growth hormone of plants. Proc Natl Acad Sci USA 18:692-701 https://doi.org/10.1073/pnas.18.12.692
  45. Vanneste S, Friml J (2009) Auxin: A trigger for change in plant development. Cell 136:1005-1016 https://doi.org/10.1016/j.cell.2009.03.001
  46. Went FW, Thimann KV (1937) Phytohormones. MacMillan, New York, USA