Abstract
A number of mutations that alter the form of the compound leaf in pea (Pisum sativum) has proven useful in elucidating the role that auxin might play in pea leaf development. The goals of this study were to determine if auxin application can rescue any of the pea leaf mutants and if gibberellic acid (GA) plays a role in leaf morphogenesis in pea. A tissue culture system was used to determine the effects of various auxins, GA or a GA biosynethesis inhibitor (paclobutrazol) on leaf development. The GA mutant, nana1 (na1) was analyzed. The uni-tac mutant was rescued by auxin and GA and rescue involved both a conversion of the terminal leaflet into a tendril and an addition of a pair of lateral tendrils. This rescue required the presence of cytokinin. The auxins tested varied in their effectiveness, although methyl-IAA worked best. The terminal tendrils of wildtype plantlets grown on paclobutrazol were converted into leaflets, stubs or were aborted. The number of lateral pinna pairs produced was reduced and leaf initiation was impaired. These abnormalities resembled those caused by auxin transport inhibitors and phenocopy the uni mutants. The na1 mutant shared some morphological features with the uni mutants; including, flowering late and producing leaves with fewer lateral pinna pairs. These results show that both auxin and GA play similar and significant roles in pea leaf development. Pea leaf morphogenesis might involve auxin regulation of GA biosynthesis and GA regulation of Uni expression.
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Abbreviations
- BA:
-
N6 -Benzylaminopurine
- 4-Cl-IAA:
-
4-Chloro-indole-3-acetic acid
- GA:
-
Gibberellic acid
- IAA:
-
Indole-3-acetic acid
- m-IAA:
-
Indole-3-acetic acid methyl ester
- MS:
-
Murashige and Skoog
- NAA:
-
α-Naphthalene-acetic acid
- NPA:
-
N-(1-Naphthyl) phthalamic acid
- PAT:
-
Polar auxin transport
- PAC:
-
(2RS,3RS)-1-(4-Chlorophenyl)-4,4-dimethyl-2-(1H-1,2,4-triazol-1-yl)-pentan-3-ol (i.e. paclobutrazol)
- PCIB:
-
p-Chlorophenoxyisobutyric acid
- SAM:
-
Shoot apical meristem
- SEM:
-
Scanning electron microscopy
- TIBA:
-
2,3,5-Triiodobenzoic acid
References
Aloni R, Schwalm K, Langhans M, Ullrich CI (2003) Gradual shifts in sites of free-auxin production during leaf-primordium development and their role in vascular differentiation and leaf morphogenesis in Arabidopsis. Planta 216:841–852
Avsian-Kretchmer O, Cheng JC, Chen L, Moctezuma E, Sung ZR (2002) Indole acetic acid distribution coincides with vascular differentiation pattern during Arabidopsis leaf ontogeny. Plant Physiol 130:199–209
Bai F, Watson JC, Walling J, Weeden N, Santner AA, DeMason DA (2005) Molecular characterization and expression of PsPK2, a PINOID-like gene from pea (Pisum sativum). Plant Sci (in press)
Benková E, Michniewicz M, Sauer M, Teichmann T, Seifertová D, Jürgens G, Friml J (2003) Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115:591–602
Blázquez MA (2000) Flower development pathways. J Cell Sci 113:3547–3548
Blázquez MA, Weigel D (2000) Integration of floral inductive signals in Arabidopsis. Nature 404:889–892
Blázquez MA, Green R, Nilsson O, Sussman MR, Weigel D (1998) Gibberellins promote flowering of Arabidopsis by activating the LEAFY promoter. Plant Cell 10:791–800
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 433:39–44
Busch A, Gleissberg S (2003) EcFLO, a FLORICAULA-like gene from Eschscholzia californica is expressed during organogenesis at the vegetative shoot apex. Planta 217:841–848
Cambridge AP, Morris DA (1996) Transfer of exogenous auxin from the phloem to the polar auxin transport pathway in pea (Pisum sativum L.) Planta 199:583–588
Chawla R, DeMason DA (2004) Molecular expression of PsPIN1, a putative auxin efflux carrier gene from pea (Pisum sativum L.). Plant Growth Reg 44:1–14
Davidson SE, Elliott RC, Helliwell CA, Poole AT, Reid JB (2003) The pea gene NA encodes ent-Kaurenoic acid oxidase. Plant Physiol 131:335–344
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, indole-3-acetic acid in suspension-cultured cells. Planta 198:532–541
DeMason DA, Chawla R (2004a) Roles for auxin during morphogenesis of the compound leaves of pea (Pisum sativum). Planta 218:435–448
DeMason DA, Chawla R (2004b) Roles of auxin and Uni in leaf morphogenesis of the afila genotype of pea (Pisum sativum). Int J Plant Sci 165:707–722
DeMason DA, Schmidt RJ (2001) Roles of the Uni gene in shoot and leaf development of pea (Pisum sativum): phenotypic characterization and leaf development in the uni and uni-tac mutants. Int J Plant Sci 162:1033–1051
DeMason DA, Villani PJ (2001) Genetic control of leaf development in pea (Pisum sativum). Int J Plant Sci 162:493–511
Friml J, Yang X, Michniewicz M, Weijers D, Quint A, Tietz O, Benjamins R, Ouwerkerk PBF, Ljung K, Sandberg G, Hooykaas PJJ, Palme K, Offringa R. (2004) A PINOID-dependent binary switch in apical-basal PIN polar targeting directs auxin efflux. Science 306: 862–865
Giles JE, Villani PJ, DeMason DA (1998) A class 1 Knox full-length cDNA from pea (Pisum sativum) shoot tips (Accession No. AF063307). Plant Physiol 117:1125
Gocal GFW, Sheldon CC, Gubler F, Moritz T, Bagnall DJ, MacMillan CP, Li SF, Parish W, Dennis ES, Weigel D, King RW (2001) GAMYB-like genes, flowering, and gibberellin signaling in Arabidopsis. Plant Physiol 127:1682–1693
Gould KS, Cutter EG, Young JPW, Charlton WA (1987) Positional differences in size, morphology and in vitro performance of pea axillary buds. Can J Bot 65:406–411
Gould KS, Cutter EG, Young JPW (1991) Modification of pea leaf morphology by 2,3,5-triiodobenzoic acid. Bot Gaz 152:133–138
Gourlay CW, Hofer JMI, Ellis THN (2000) Pea compound leaf architecture is regulated by interactions among the genes Unifoliata,Cochleata, Afila, and Tendril-less. Plant Cell 12:1279–1294
Hamann T, Mayer U, Jürgens G (1999) The auxin-insensitive bodenlos mutation affects primary root formation and apical-basal patterning in the Arabidopsis embryo. Development 126:1387–1395
Hamann T, Benkova E, Bäurle T, Kientz M, Jürgens G (2002) The Arabidopsis BODENLOS gene encodes an auxin response protein inhibiting MONOPTEROS-mediated embryo patterning. Genes Dev 16:1610–1615
Hay A, Kaur H, Phillips A, Hedden P, Hake S, Tsiantis M (2002) The gibberellin pathway mediates KNOTTED1-type homeobox function in plants with different body plans. Curr Biol 12:1557–1565
Hay A, Jackson D, Ori N, Hake S (2003) Analysis of the competence to respond to KNOTTED1 activity in Arabidopsis leaves using a steroid induction system. Plant Physiol 131:1671–1680
Hay A, Craft J, Tsiantis M. (2004) Plant hormones and homeoboxes: bridging the gap? BioEssays 26:395–404
Hofer J, Turner L, Hellens R, Ambrose M, Matthews P, Michael A, Ellis N (1997) UNIFOLIATA regulates leaf and flower morphogenesis in pea. Curr Biol 7:581–587
Hofer J, Gourlay C, Michael A, Ellis THN (2001) Expression of a class 1 knotted1-like homeobox gene is down-regulated in pea compound leaf primordia. Plant Mol Biol 45:387–398
van Huizen R, Ozga JA, Reinecke DM (1997) Seed and hormonal regulation of gibberellin 20-oxidase expression in pea pericarp. Plant Physiol 115:123–128
Keller CP, Stahlberg R, Barkawi LS, Cohen JD (2004) Long-term inhibition by auxin of leaf blade expansion in bean and Arabidopsis. Plant Physiol 134:1217–1226
Kusaba S, Kano-Murakami Y, Matsuoka M, Tamaoki M, Sakamoto T, Yamaguchi I, Fukumoto M (1998) Alteration of hormone levels in transgenic tobacco plants overexpressing the rice homeobox gene OSH1. Plant Physiol 116:471–476
Lamprecht H (1933) Ein Unifoliata-Typ von Pisum mit gleichzeitiger Pistilloidie. Hereditas 18:56–64
Li C, Bangerth F (2003) Stimulatory effect of cytokinins and interactions with IAA on the release of lateral buds of pea plants from apical dominance. J Plant Physiol 160:1059–1063
Ljung K, Bhalerao RP, Sandberg G (2001) Sites and homeostic control of auxin biosynthesis in Arabidopsis during vegetative growth. Plant J 28:465–474
Lu B, Villani PJ, Watson JC, DeMason DA, Cooke TJ (1996) The control of pinna morphology in wildtype and mutant leaves of the garden pea (Pisum sativum L). Int J Plant Sci 157:659–673
Marx GA (1987) A suite of mutants that modify pattern formation in pea leaves. Plant Mol Biol Rep 5:311–335
Mattsson J, Ckurshumova W, Berleth T (2003) Auxin signaling in Arabidopsis leaf vascular development. Plant Physiol 131:1327–1339
Miyawaki K, Matsumoto-Kitano M, Kakimoto T (2004) Expression of cytokinin biosynthetic isopentenyltransferase genes in Arabidopsis: tissue specificity and regulation by auxin cytokinin and nitrate. Plant J 37:128–138
Morris DA, Thomas AG (1978) A microautoradiographic study of auxin transport in the stem of inteact pea seedlings (Pisum sativum L.). J Exp Bot 29:147–157
Ngo P, Ozga JA, Reinecke DM (2002) Specificity of auxin regulation of gibberellin 20-oxidase gene expression in pea pericarp. Plant Mol Biol 49:439–448
Nordström A, Tarkowski P, Tarkowska D, Norbaek R, Åstot C, Dolezal K, Sandberg G (2004) Auxin regulation of cytokinin biosynthesis in Arabidopsis thaliana: a factor of potential importance for auxin-cytokinin-regulated development. Proc Natl Acad Sci U S A 101:8039–8044
O’Brien TP, McCully ME (1981) The study of plant structure: principles and selected methods. Termararpchi Pty Ltd, Melbourne, Australia
O’Neill DP, Ross JJ (2002) Auxin regulation of the gibberellin pathway in pea. Plant Physiol 130:1974–1982
Ozga JA, Reinecke DM (1999) Interactions of 4-chloroindole-3-acetic acid and gibberellins in early fruit development. Plant Growth Reg 27:33–38
Polit JT, Maszewski J, Kaźmierczak A (2003) Effect of BAP and IAA on the expression of G1 and G2 control points and G1-S and G2-M transitions in root meristem cells of Vicia faba. Cell Biol Int 27:559–566
Reid JB, Ross JJ (1993) A mutant based approach, using Pisum sativum, to understand plant growth. Int J Plant Sci 154:22–34
Reinecke DM (1999) 4-Chloroindole-3-acetic acid and plant growth. Plant Growth Reg 27:3–13
Reinecke DM, Ozga JA, Ilić N, Magnus V, Kojić-Prodić B (1999) Molecular properties of 4-substituted indole-3-acetic acids affecting pea pericarp elongation. Plant Growth Reg 27:39–48
Reinhardt D, Pesce ER, Stieger P, Mandel T, Baltensperger K, Bennett M, Traas J, Friml J, Kuhlemeier C (2003) Regulation of phyllotaxis by polar auxin transport. Nature 426:255–260
Ross JJ, Murfet IC, Reid JB (1997) Gibberellin mutants. Physiol Plant 100:550–560
Ross JJ, O’Neill DP, Smith JJ, Huub L, Kerckhoff J, Elliott RC (2000) Evidence that auxin promotes gibberellin A1 biosynthesis in pea. Plant J 21:547–552
Ross JJ, Davidson SE, Wolbang CM, Bayly-Stark E, Smith JJ, Reid JB (2003) Developmental regulation of the gibberellin pathway in pea shoots. Funct Plant Biol 30:83–89
Sabatini S, Beis D, Wolkenfelt H, Murfett J, Guilfoyle T, Malamy J, Benfey P, Leyser O, Bechtold N, Weisbeek P, Scheres B (1999) An auxin-dependent distal organizer of pattern and polarity in the Arabidopsis root. Cell 99:463–472
Sakamoto T, Kamiya N, Ueguchi-Tanaka M, Iwahori S, Matsuoka M (2001) KNOX homeodomain protein directly suppresses the expression of a gibberellin biosynthetic gene in the tobacco shoot apical meristem. Genes Dev 15:581–590
Scheres B (2000) Non-linear signaling for pattern formation? Curr Opin Plant Biol 3:412–417
Sharma B (1972) “Tendrilled acacia”, a new mutation controlling tendril formation in Pisum sativum. Pisum Newslett 4:50
Sharma B (1981) Genetic pathway of foliage development in Pisum sativum. Pulse Crops Newslett 1:56–57
Steinmann T, Geldner N, Grebe M, Mangold S, Jackson CL, Paris S, Gälweiler L, Palme K, Jürgens G (1999) Coordinated polar localization of auxin efflux carrier PIN1 by Gnom ARF GEF. Science 286:316–318
Tanaka-Ueguchi M, Itoh H, Oyama N, Koshioka M, Matsuoka M (1988) Over-expression of a tobacco homeobox gene, NTH15, decreases the expression of a gibberellin biosynthetic gene encoding GA 20-oxidase. Plant J 15:391–400
Uggla C, Moritz T, Sandberg G, Sundberg C (1996) Auxin as a positional signal in pattern formation in plants. Proc Natl Acad Sci U S A 93:9282–9286
Villani PJ, DeMason DA (1997) Roles of the Af and Tl genes in pea leaf morphogenesis: characterization of the double mutant (afaftltl). Am J Bot 84:1323–1336
Villani PJ, DeMason DA (1999) Roles of the Af and Tl genes in pea leaf morphogenesis: leaf morphology and pinna anatomy of the heterozygotes. Can J Bot 77:611–622
Werner T, Motyka V, Laucou V, Smets R, Van Onckelen H, Schmülling T (2003) Cytokinin-deficient transgenic Arabidopsis plants show multiple developmental alternations indicating opposite functions of cytokinins in the regulation of shoot and root meristem activity. Plant Cell 15:2532–2550
Willemsen V, Friml J, Grebe M, van den Toorn A, Palme K, Scheres B (2003) Cell polarity and PIN protein positioning in Arabidopsis require STEROL METHYLTRANSFERASE1 function. Plant Cell 15: 612–625
Yip W, Yang SFB (1986) Effect of thidiazuron, a cytokinin-active urea derivative, in cytokinin-dependent ethylene production systems. Plant Physiol 80:515–519
Acknowledgements
The author thanks Janet Giles and Fang Bai for their technical assistance with the tissue culture. I thank Dr. Gene Nothnagel for determining the PAC concentration of the ICI product. I also acknowledge Jerry Cohen for providing the 4-Cl-IAA used and for many lively discussions. Dr. Lewis Mander provided the GA1. The SEM was done in the Analytical Microscopy facility at the University of California, Riverside. Dr. Patty Springer provided a critical reading of the manuscript. The work was supported by a grant from USDA/NRI 2001-35304-10958.
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DeMason, D.A. Auxin–cytokinin and auxin–gibberellin interactions during morphogenesis of the compound leaves of pea (Pisum sativum). Planta 222, 151–166 (2005). https://doi.org/10.1007/s00425-005-1508-6
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DOI: https://doi.org/10.1007/s00425-005-1508-6