Abstract
The shoot of grass coleoptiles consists of the mesocotyl, the node, and the coleoptile (with enclosed primary leaf). Since the 1930s, it is known that auxin (indole-3-acetic acid, IAA), produced in the tip of the coleoptile, is the central regulator of turgor-driven organ growth. Fifty years ago, it was discovered that antibiotics that suppress protein biosynthesis, such as cycloheximide, inhibit auxin (IAA)-induced cell elongation in excised sections of coleoptiles and stems. Based on such inhibitor studies, the concept of “growth-limiting proteins (GLPs)” emerged that was subsequently elaborated and modified. Here, we summarize the history of this idea with reference to IAA-mediated shoot elongation in maize (Zea mays) seedlings and recent studies on the molecular mechanism underlying auxin action in Arabidopsis thaliana. In addition, the analysis of light-induced inhibition of shoot elongation in intact corn seedlings is discussed. We propose a concept to account for the GLP-mediated epidermal wall-loosening process in coleoptile segments and present a more general model of growth regulation in intact maize seedlings. Quantitative proteomic and genomic studies led to a refinement of the classic “GLP concept” to explain phytohormone-mediated cell elongation at the molecular level (i.e., the recently proposed theory of a “central growth regulation network,” CGRN). Novel data show that mesocotyl elongation not only depends on auxin but also on brassinosteroids (BRs). However, the biochemical key processes that regulate the IAA/BR-mediated loosening of the expansion-limiting epidermal wall(s) have not yet been elucidated.
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References
Abel S, Theologis A (2010) Odyssey of auxin. Cold Spring Harb Perspect Biol 2:1–10
Bai M-Y, Shang J-Y, Oh E, Fan M, Bai Y, Zentella R, Sun T-P, Wang Z-Y (2012a) Brassinosteroid, gibberellin and phytochrome impinge on a common transcription module in Arabidopsis. Nat Cell Biol 14:810–817
Bai M-Y, Fan M, Oh E, Wang Z-Y (2012b) A triple helix-loop-helix/basic helix-loop-helix cascade controls cell elongation downstream of multiple hormonal and environmental signalling pathways in Arabidopsis. Plant Cell 24:4917–4929
Barker-Bridgers M, Ribnicky DM, Cohen JD, Jones AM (1998) Red-light-regulated growth. Changes in the abundance of indole-acetic acid in maize (Zea mays L.) mesocotyl. Planta 204:207–211
Baskin TI (2005) Anisotropic expansion of the plant cell wall. Annu Rev Cell Dev Biol 21:203–222
Bates GW, Cleland RE (1979) Protein synthesis and auxin-induced growth: inhibitor studies. Planta 145:437–442
Becker D, Hedrich R (2002) Channelling auxin action: modulation of ion transport by indole-3-acetic acid. Plant Mol Biol 49:349–356
Benjamins R, Scheres B (2008) Auxin: the looping star in plant development. Annu Rev Plant Biol 59:443–465
Bergfeld R, Speth V, Schopfer P (1988) Reorientation of microfibrils and microtubules at the outer epidermal wall of maize coleoptiles during auxin-mediated growth. Bot Acta 101:57–67
Borucka J, Fellner M (2012) Auxin binding proteins ABP1 and ABP4 are involved in the light- and auxin-induced down-regulation of phytochrome gene PHYB in maize (Zea mays L.) mesocotyl. Plant Growth Regul 68:503–509
Briggs WR (2014) Phototropism: some history, some puzzles, and a look ahead. Plant Physiol 164:13–23
Brummell DA, Hall JL (1987) Rapid cellular responses to auxin and the regulation of growth. Plant Cell Environ 10:523–543
Burdach Z, Kurtyka R, Siemieniuk A, Karcz W (2014) Role of chloride ions in the promotion of auxin-induced growth of maize coleoptiles. Ann Bot 114:1023–1034
Chae K, Isaacs CG, Reeves PH, Maloney GS, Muday GR, Nagpal P, Reed JW (2012) Arabidopsis SMALL AUXIN UP RNA 63 promotes hypocotyl and stamen filament elongation. Plant J 71:684–697
Chan J (2012) Microtubule and cellulose microfibril orientation during plant cell and organ growth. J Microsc 247:23–32
Chapman EJ, Estelle M (2009) Mechanism of auxin-regulated gene expression in plants. Annu Rev Genet 43:265–285
Chung Y, Choe S (2013) The regulation of brassinosteroid biosynthesis in Arabidopsis. Crit Rev Plant Sci 32:396–410
Claussen M, Luthen H, Blatt M, Bottger M (1997) Auxin-induced growth and its linkage to potassium channels. Planta 201:227–234
Cleland RE (1971) Instability of the growth-limiting proteins of the Avena coleoptile and their pool size in relation to auxin. Planta 99:1–11
Cona A, Cenci F, Cervelli M, Federico R, Mariottini P, Moreno S, Angelini R (2003) Polyamine oxidase, a hydrogen peroxide-producing enzyme, is up-regulated by light and down-regulated by auxin in the outer tissues of the maize mesocotyl. Plant Physiol 131:803–813
Cosgrove DJ (1997) Relaxation in a high-stress environment: the molecular bases of extensible cell walls and cell enlargement. Plant Cell 9:1031–1041
Cosgrove DJ (2005) Growth of the plant cell wall. Nat Rev Mol Cell Biol 6:850–861
Deng Z, Xu S, Chalkley RJ, Oses-Prieto JA, Burlingame AL, Wang Z-Y, Kutschera U (2012) Rapid auxin-mediated changes in the proteome of the epidermal cells in rye coleoptiles: implications for the initiation of growth. Plant Biol 14:420–427
Deng Z, Oses-Prieto JA, Kutschera U, Tseng T-S, Hao L, Burlingame AL, Wang Z-Y, Briggs WR (2014) Blue light-induced proteomic changes in etiolated Arabidopsis seedlings. J Proteome Res 13:2524–2533
Dietz A, Kutschera U, Ray PM (1990) Auxin enhancement of mRNAs in epidermis and internal tissues of the pea stem and its significance for control of elongation. Plant Physiol 93:432–438
Dubois PG, Olsefski GT, Flint-Garcia S, Setter TL, Hoekenga OA, Brutnell TP (2010) Physiological and genetic characterization of end-of-day far-red light response in maize seedlings. Plant Physiol 154:173–186
Edelmann HG, Kutschera U (1993) Rapid auxin-induced enhancement of protein biosynthesis in rye coleoptiles. J Plant Physiol 142:343–346
Edelmann HG, Schopfer P (1989) Role of protein and RNA synthesis in the inhibition of auxin-mediated growth in coleoptiles of Zea mays L. Planta 179:475–485
Edelmann HG, Bergfeld R, Schopfer P (1995) Effect of inhibition of protein glycosylation on auxin-induced growth and the occurrence of osmiophilic particles in maize (Zea mays L.) coleoptiles. J Exp Bot 46:1745–1752
Edelmann HG, Neinhuis C, Bargel H (2005) Influence of hydration and temperature on the rheological properties of plant cuticles and their impact on plant organ integrity. J Plant Growth Regul 24:116–126
Fan M, Bai M-Y, Kim J-G, Wang T, Oh E, Chen L, Park CH, Son S-H, Kim S-K, Mudgett MB, Wang Z-Y (2014) The bHLH transcription factor HBI1 mediates the trade-off between growth and pathogen-associated molecular pattern-triggered immunity in Arabidopsis. Plant Cell 26:828–841
Frankova L, Fry SC (2013) Biochemistry and physiological roles of enzymes that ‘cut and paste’ plant cell-wall polysaccharides. J Exp Bot 64:3519–3550
Gao Q, Zhao M, Li F, Guo Q, Xing S, Wang W (2008) Expansins and coleoptile elongation in wheat. Protoplasma 233:73–81
Georgelis N, Yennawar NH, Cosgrove DJ (2012) Structural basis for entropy-driven cellulose binding by a type-A cellulose-binding module (CBN) and bacterial expansins. Proc Natl Acad Sci U S A 109:14830–14835
Goda H, Sawa S, Asami T, Fujioka S, Shimada Y, Yoshida S (2004) Comprehensive comparison of auxin-regulated and brassinosteroid-regulated genes in Arabidopsis. Plant Physiol 130:1319–1334
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
Hao J, Yin Y, Fei S (2013) Brassinosteroid signalling network: implications on yield and stress tolerance. Plant Cell Rep 32:1017–1030
Hartwig T, Chuck GS, Fujioka S, Klempien A, Weizbauer R, Potluri DPV, Choe S, Johal GS, Schulz B (2011) Brassinosteroid control of sex determination in maize. Proc Natl Acad Sci U S A 108:19814–19819
Hartwig T, Corvalan C, Best NB, Budka JS, Zhu J-Y, Choe S, Schulz B (2012) Propiconazole is a specific and accessible brassinosteroid (BR) biosynthesis inhibitor for Arabidopsis and maize. PLoS ONE 7/5:e36625
Hoffmann-Benning S, Klomparens KL, Kende H (1994) Characterization of growth-related osmiophilic particles in corn coleoptiles and deepwater rice internodes. Ann Bot 74:563–572
Iino M (1982) Inhibitory action of red light on the growth of the maize mesocotyl: evaluation of the auxin hypothesis. Planta 156:388–395
Iino M, Carr DJ (1982) Sources of free IAA in the mesocotyl of etiolated maize seedlings. Plant Physiol 69:1109–1112
Jones AM, Cochran DS, Lamerson PM, Evans ML, Cohen JD (1991) Red light-regulated growth. I. Changes in the abundance of indoleacetic acid and 22-kilodalton auxin-binding protein in the maize mesocotyl. Plant Physiol 97:352–358
Karcz W, Burdach Z (2007) Effect of temperature on growth, proton extrusion and membrane potential in maize (Zea mays L.) coleoptile segments. Plant Growth Regul 52:141–150
Key JL (1964) Ribonucleic acid and protein synthesis are essential processes for cell elongation. Plant Physiol 39:365–370
Key JL (1969) Hormones and nucleic acid metabolism. Annu Rev Plant Physiol 20:449–474
Key JL, Ingle J (1964) Requirement for the synthesis of DNA-like RNA for the growth of excised plant tissue. Proc Natl Acad Sci U S A 52:1382–1388
Key JL, Shannon JC (1964) Enhancement by auxin of ribonucleic acid synthesis in excised soybean hypocotyl tissue. Plant Physiol 39:360–364
Kim T-W, Wang Z-Y (2010) Brassinosteroid signal transduction from receptor kinases to transcription factors. Annu Rev Plant Biol 61:681–704
Kim Y-S, Kim T-W, Kim S-K (2005) Brassinosteroids are inherently biosynthesized in the primary roots of maize, Zea mays L. Phytochemistry 66:1000–1006
Kriechbaumer V, Park WJ, Gierl A, Glawischnig E (2006) Auxin biosynthesis in maize. Plant Biol 8:334–339
Kutschera U (1994) The current status of the acid-growth hypothesis. New Phytol 126:549–569
Kutschera U (2001) Stem elongation and cell wall proteins in flowering plants. Plant Biol 3:466–480
Kutschera U (2003) Auxin-induced cell elongation in grass coleoptiles: a phytohormone in action. Curr Topics Plant Biol 4:27–46
Kutschera U (2006) Acid growth and plant development. Science 311:952–953
Kutschera U (2008a) The outer epidermal wall: design and physiological role of a composite structure. Ann Bot 101:615–621
Kutschera U (2008b) The pacemaker of plant growth. Trends Plant Sci 13:105–107
Kutschera U, Briggs WR (2009) From Charles Darwin's botanical country-house studies to modern plant biology. Plant Biol 11:785–795
Kutschera U, Briggs WR (2012) Root phototropism: from dogma to the mechanism of blue light perception. Planta 235:443–452
Kutschera U, Briggs WR (2013) Seedling development in buckwheat and the discovery of the photomorphogenic shade-avoidance response. Plant Biol 15:931–940
Kutschera U, Edelmann HG (2005) Osmiophilic nanoparticles in epidermal cells of grass coleoptiles: implications for growth and gravitropism. Rec Res Dev Plant Sci 3:1–14
Kutschera U, Niklas KJ (2007) The epidermal-growth-control theory of stem elongation: an old and a new perspective. J Plant Physiol 164:1395–1409
Kutschera U, Niklas KJ (2009) Evolutionary plant physiology: Charles Darwin's forgotten synthesis. Naturwissenschaften 96:1339–1354
Kutschera U, Niklas KJ (2013) Cell division and turgor-driven stem elongation in juvenile plants: a synthesis. Plant Sci 207:45–56
Kutschera U, Schopfer P (1986) Effect of auxin and abscisic acid on cell wall extensibility in maize coleoptiles. Planta 167:527–535
Kutschera U, Wang Z-Y (2012) Brassinosteroid action in flowering plants: a Darwinian perspective. J Exp Bot 63:3511–3522
Kutschera U, Bergfeld R, Schopfer P (1987) Cooperation of epidermis and inner tissues in auxin-mediated growth of maize coleoptiles. Planta 170:168–180
Kutschera U, Deng Z, Oses-Prieto JA, Burlingame AL, Wang Z-Y (2010) Cessation of coleoptile elongation and loss of auxin sensitivity in developing rye seedlings. A quantitative proteomic analysis. Plant Signal Behav 5:509–517
Lamport DTA, Kieliszewski MJ, Chen Y, Cannon MC (2011) Role of the extensin superfamily in primary cell wall architecture. Plant Physiol 156:11–19
Lamport DTA, Varnail P, Seal C (2014) Back to the future with the AGP-Ca2+ flux capacitor. Ann Bot 114:1069–1085
Li J, Dickerson TJ, Hoffmann-Benning S (2013) Contribution of proteomics in the identification of novel proteins associated with plant growth. J Proteome Res 12:4882–4891
Lipchinsky A (2013) How do expansins control plant growth? A model for cell wall loosening via defect migration in cellulose microfibrils. Acta Physiol Plant 35:3277–3284
Lipchinsky A, Sharova EL, Medvedev SS (2013) Elastic properties of the growth-controlling outer cell walls of maize coleoptile epidermis. Acta Physiol Plant 35:2183–2191
Ljung K (2013) Auxin metabolism and homeostasis during plant development. Development 140:943–950
Makarevitch I, Thompson A, Muehlbauer GJ, Springer NM (2012) Brd1 gene in maize encodes a brassinosteroid C-6 oxidase. PLoS ONE 7:e30798
Markelz NH, Costich DE, Brutnell TP (2003) Photomorphogenic responses in maize seedling development. Plant Physiol 133:1574–1591
McQueen-Mason S, Durachko DM, Cosgrove DJ (1992) Two endogenous proteins that induce cell wall extension in plants. Plant Cell 4:1425–1433
Mer CL (1951) A critical study of the auxin theory of growth regulation in the mesocotyl of Avena sativa. Ann Bot 15:179–207
Mori Y, Nishimura T, Koshiba T (2005) Vigorous synthesis of indole-3-acetic acid in the very apical tip leads to a constant basipedal flow of the hormone in maize coleoptiles. Plant Sci 164:467–473
Nemhauser JL, Mockler TC, Chory J (2004) Interdependency of brassinosteroid and auxin signalling in Arabidopsis. PLoS Biol 2:e258
Niklas KJ, Kutschera U (2009) The evolutionary development of plant body plans. Funct Plant Biol 36:682–695
Niklas KJ, Kutschera U (2010) The evolution of the land plant life cycle. New Phytol 185:27–41
Niklas KJ, Kutschera U (2012) Plant development, auxin, and the subsystem incompleteness theorem. Front Plant Sci 3(37):1–11
Nishimura T, Toyooka K, Sato M, Matsumoto S, Lucas MM, Stonad M, Baluska F, Koshiba T (2011) Immunohistochemical observation of indole-3-acetic acid at the IAA synthetic maize coleoptile tip. Plant Signal Behav 6:2013–2022
Noodén LD, Thimann KV (1963) Evidence for a requirement for protein synthesis for auxin-induced cell enlargement. Proc Natl Acad Sci U S A 50:194–200
Oh E, Zhu J-Y, Bai M-Y, Arenhart RA, Sun Y, Wang Z-Y (2014) Cell elongation is regulated through a central circuit of interacting transcription factors in the Arabidopsis hypocotyl. eLife 10:7554
Okamoto-Nakazato A (2002) A brief note on yieldin, a wall-bound protein that regulates the yield threshold of the cell wall. J Plant Res 115:309–313
Olivier NB (2014) Structural biology: ribosome revelations. Nature 513:491–492
Penny P (1971) Growth-limiting proteins in relation to auxin-induced elongation in lupin hypocotyls. Plant Physiol 48:720–723
Rudnicka M, Polak M, Karcz W (2014) Cellular responses to naphthoquinones: juglone as a case study. Plant Growth Regul 72:239–248
Samajova O, Samaj J, Volkmann D, Edelmann HG (1998) Occurrence of osmiophilic particles is correlated to elongation growth in higher plants. Protoplasma 202:185–191
Savaldi-Goldstein S, Peto C, Chory J (2007) The epidermis both drives and restricts plant shoot growth. Nature 446:199–202
Schindler T, Bergfeld R, Hohl M, Schopfer P (1994) Inhibition of Golgi-apparatus function by brefeldin A in maize coleoptiles and its consequences on auxin-mediated growth, cell-wall extensibility and secretion of cell-wall proteins. Planta 192:404–413
Schneider-Poetsch T, Ju J, Eyler DE, Dang Y, Bhat S, Merrick WC, Green R, Shen B, Liu JO (2010) Inhibition of eukaryotic translation elongation by cycloheximide and lactimidomycin. Nat Chem Biol 6:209–217
Schopfer P (1993) Determination of auxin-dependent pH changes in coleoptile cell walls by a null-point method. Plant Physiol 103:351–357
Schopfer P (2006) Biomechanics of plant growth. Am J Bot 93:1415–1425
Schopfer P, Lapierre C, Nolte T (2001) Light-controlled growth of the maize seedling mesocotyl: Mechanical cell-wall changes in the elongation zone and related changes in lignification. Physiol Plant 111:83–92
Sekimata K, Han SY, Yoneyama K, Takeuche Y, Yoshida S et al (2002) A specific and potent inhibitor of brassinosteroid biosynthesis possessing a dioxolane ring. J Agric Food Chem 50:3486–3490
Shannon JC, Hanson JB, Wilson CM (1964) Ribonuclease levels in the mesocotyl tissue of Zea mays as a function of 2,4-dichlorophenoxyacetic acid application. Plant Physiol 39:804–809
Shishova M, Lindberg S (2010) A new perspective on auxin perception. J Plant Physiol 167:417–422
Song Y (2014) Insights into the mode of action of 2,4-dichlorophenoxyacetic acid (2,4-D) as an herbicide. J Integr Plant Biol 56:106–113
Srivastava LM (2002) Plant growth and development. Hormones and environment. Academic, San Diego
Stevenson TT, Cleland RE (1981) Osmoregulation in the Avena coleoptile in relation to auxin and growth. Plant Physiol 67:749–753
Takahashi K, Hayashi K, Kinoshita T (2012) Auxin activates the plasma membrane H+-ATPase by phosphorylation during hypocotyl elongation in Arabidopsis. Plant Physiol 159:2632–2641
Teale WD, Poponov IA, Palme K (2006) Auxin in action: signaling, transport and the control of plant growth and development. Nat Rev Mol Cell Biol 7:847–859
Valdivia ER, Wu Y, Li L-C, Cosgrove DJ, Stephenson AG (2007) A group-1 grass pollen allergen influences the outcome of pollen competition in maize. PLoS ONE 2(1):e154
van Overbeek J (1936) Growth hormone and mesocotyl growth. Rec Trav Bot Neerl 33:333–340
Vanderhoef LN, Briggs WR (1978) Red light-inhibited mesocotyl elongation in maize seedlings. 1. The auxin hypothesis. Plant Physiol 61:534–537
Vaughn KC (2002) Attachment of the parasitic weed dodder to the host. Protoplasma 219:227–237
Visnovitz T, Touati M, Miller AJ, Fricke W (2013) Apoplast acidification in growing barley (Hordeum vulgare L.) leaves. J Plant Growth Regul 32:131–139
Walcher CL, Nemhauser JL (2012) Bipartite promoter element required for auxin response. Plant Physiol 158:273–282
Wang Z-Y (2012) Brassinosteroids modulate plant immunity at multiple levels. Proc Natl Acad Sci U S A 109:7–8
Wang Z-Y, Bai M-Y, Oh E, Zhu J-Y (2012) Brassinosteroid signaling network and regulation of photomorphogenesis. Annu Rev Genet 46:701–724
Wang W, Bai M-Y, Wang Z-Y (2014) The brassinosteroid signaling network—a paradigm of signal integration. Curr Opin Plant Biol 21:147–153
Went FW (1928) Wuchsstoff und Wachstum. Rec Trav Bot Neerl 25:1–116
Went FW, Thimann KV (1937) Phytohormones. The Macmillan Company, New York
Woodward AW, Bartel B (2005) Auxin: regulation, action, and interaction. Ann Bot 95:707–735
Xu T, Wen M, Nagawa S, Fu Y, Chen JG, Wu MJ, Perrot-Rechenmann C, Friml J, Jones AM, Yang Z (2010) Cell surface and rho GTPase-based auxin signaling controls cellular integration in Arabidopsis. Cell 143:99–110
Yahalom A, Epel BL, Glinka Z, MacDonald IR, Gordon DC (1987) A kinetic analysis of phytochrome controlled mesocotyl growth in Zea mays seedlings. Plant Physiol 84:390–394
Yahalom A, Epel BL, Glinka Z (1988) Photomodulation of mesocotyl elongation in maize seedlings: is there a correlative relationship between phytochrome, auxin and cell wall extensibility? Physiol Plant 72:428–433
Zažimalovà E, Petràšek J, Benkovà (eds) (2014) Auxin and its role in plant development. Springer, Wien
Zhao Y (2012) Auxin biosynthesis: a simple two-step pathway converts tryptophan to indole-3-acetic acid in plants. Mol Plant 5:334–338
Zhao M-R, Li F, Fang Y, Gao Q, Wang W (2011) Expansin-regulated cell elongation is involved in the drought tolerance of wheat. Protoplasma 248:313–323
Zhu J-Y, Sae-Seaw J, Wang Z-Y (2013) Brassinosteroid signalling. Development 140:1615–1620
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This project was supported by the Alexander von Humboldt-Stiftung (AvH fellowships Stanford 2012/13 to UK, Institute of Biology, University of Kassel, Germany) and grants from the US National Institute of Health (R01GM066258 to Z.-Y. W.).
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Kutschera, U., Wang, ZY. Growth-limiting proteins in maize coleoptiles and the auxin-brassinosteroid hypothesis of mesocotyl elongation. Protoplasma 253, 3–14 (2016). https://doi.org/10.1007/s00709-015-0787-4
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DOI: https://doi.org/10.1007/s00709-015-0787-4