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Comprehensive hormone profiling of the developing seeds of four grain legumes

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Abstract

Key message

Developmental context and species-specific hormone requirements are of key importance in the advancement of in vitro protocols and manipulation of seed development.

Abstract

Improvement of in vitro tissue and cell culture protocols in grain legumes such as embryo rescue, interspecific hybridization, and androgenesis requires an understanding of the types, activity, and balance of hormones within developing seeds. Towards this goal, the concentration of auxin, cytokinin, gibberellin, and abscisic acid (ABA) and their precursors and derivatives were measured in the developing seeds of field pea (Pisum sativum L.), chickpea (Cicer arietinum L.), lentil (Lens culinaris Medik.), and faba bean (Vicia faba L.) from 4 days after anthesis until 8 days after reaching maximum fresh weight. The importance of developmental context (developmental time and space) is demonstrated in both the differences and similarities between species for hormone profiles, especially with regard to cytokinin and ABA biosynthesis during the embryo formation. Auxin and its conjugates are significant during the pattern formation stage of all legumes; however, IAA-Asparagine appears important in the Vicieae species and its concentrations are greater than IAA from the globular stage of embryo development on in multi-seed fruits. Finally, the significance of non-polar gibberellins during lentil seed development is highlighted.

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References

  • Alabadi D, Blázquez MA, Carbonell J, Ferrándiz C, Pérez-Amador MA (2009) Instructive roles for hormones in plant development. Int J Dev Biol 53:1597–1608

    Article  PubMed  CAS  Google Scholar 

  • Bajguz A, Piotrowska A (2009) Conjugates of auxin and cytokinin. Phytochem 70:957–969

    Article  CAS  Google Scholar 

  • Braybrook SA, Harada JJ (2008) LECs go crazy in embryo development. Trends Plant Sci 13:624–630

    Article  PubMed  CAS  Google Scholar 

  • Campanella JJ, Smith SM, Leibu D, Wexler S, Ludwig-Muller J (2008) The auxin conjugate hydrolase family of Medicago truncatula and their expression during the interaction with two symbionts. J Plant Growth Regul 27:26–38

    Google Scholar 

  • Chiwocha SDS, Abrams SR, Ambrose SJ, Cutler AJ, Loewen M, Ross ARS, Kermode AR (2003) A method for profiling classes of plant hormones and their metabolites using liquid chromatography-electrospray ionization tandem mass spectrometry: analysis of hormone regulation of thermodormancy of lettuce (Lactuca sativa L.) seeds. Plant J 3:405–417

    Article  Google Scholar 

  • Chiwocha SDS, Cutler AJ, Abrams SR, Ambrose SJ, Yang J, Ross ARS, Kermode AR (2005) The etr1-2 mutation in Arabidopsis thaliana affects the abscisic acid, auxin, cytokinin and gibberellin metabolic pathways during maintenance of seed dormancy, moist-chilling and germination. Plant J 42:35–48

    Article  PubMed  CAS  Google Scholar 

  • Clarke HJ, Wilson JG, Kuo I, Lulsdorf MM, Mallifkarjuna N, Kuo J, Siddique KHM (2006) Embryo rescue and plant regeneration in vitro of selfed chickpea (Cicer arietinum L.) and its wild annual relatives. Plant Cell Tissue Organ Cult 85:197–204

    Article  Google Scholar 

  • Croser JS, Lulsdorf MM, Davies PA, Clarke HJ, Bayliss KL, Mallikarjuna N, Siddique KHM (2006) Toward doubled haploid production in the Fabaceae: progress, constraints, and opportunities. CRC Crit Rev Plant Sci 25:139–157

    Article  Google Scholar 

  • Dorcey E, Urbez C, Blazquez MA, Carbonell J, Perez-Amador MA (2009) Fertilization-dependent auxin response in ovules triggers fruit development through the modulation of gibberellin metabolism in Arabidopsis. Plant J 58:318–332

    Article  PubMed  CAS  Google Scholar 

  • Emery RJN, Leport L, Barton JE, Turner NC, Atkins CA (1998) cis-Isomers of cytokinins predominate in chickpea seeds throughout their development. Plant Physiol 117:1515–1523

    Article  PubMed  CAS  Google Scholar 

  • Emery RJN, Ma Q, Atkins CA (2000) The forms and sources of cytokinins in developing white lupine seeds and fruits. Plant Physiol 123:1593–1604

    Article  PubMed  CAS  Google Scholar 

  • Engvild KC, Egsgaard H, Larsen E (1981) Determination of 4-chloroindoleacetic acid methyl ester in Viciae species by gas chromatography-mass spectrometry. Physiol Plant 53:79–81

    Article  CAS  Google Scholar 

  • Environment Canada (2013) National climate data and information archive—Saskatoon, Government of Canada http://www.climate.weatheroffice.gc.ca/climateData/dailydata_e.html?timeframe=4&Prov=SK&StationID=47707&Month=6&Day=5&Year=2012

  • Hampson CR, Reaney MJT, Abrams GD, Abrams SR, Gusta LV (1992) Metabolism of (+)-Abscisic acid to (+)-7′-hydroxyabscisic acid by bromegrass cell cultures. Phytochemistry 31:2645–2648

    Article  CAS  Google Scholar 

  • Hwang I, Sheen J, Muller B (2012) Cytokinin signaling networks. Annu Rev Plant Biol 63:353–380

    Article  PubMed  CAS  Google Scholar 

  • Jadhav AS, Taylor DC, Giblin M, Ferrie AMR, Ambrose SJ, Ross ARS, Nelson KM, Zaharia LI, Sharma N, Anderson M, Fobert PR, Abrams SR (2008) Hormonal regulation of oil accumulation in brassica seeds: metabolism and biological activity of ABA, 7′-, 8′- and 9′-hydroxy ABA in microspore derived embryos of B. napus. Phytochemistry 69:2678–2688

    Google Scholar 

  • Jenik PD, Barton MK (2005) Surge and destroy: the role of auxin in plant embryogenesis. Development 132(16):3577–3585

    Article  PubMed  CAS  Google Scholar 

  • Kanno Y, Jikumaru Y, Hanada A, Nambara E, Abrams S, Kamiya Y, Seo M (2010) Comprehensive hormone profiling in developing Arabidopsis seeds: examination of the site of ABA biosynthesis, ABA transport and hormone interactions. Plant Cell Physiol 51(12):1988–2001

    Article  PubMed  CAS  Google Scholar 

  • Kieber JJ, Schaller GE (2010) The perception of cytokinin: a story 50 years in the making. Plant Physiol 154:487–492

    Article  PubMed  CAS  Google Scholar 

  • Liu B, Liu X, Wang C, Jin J, Herbert SJ (2010) Endogenous hormones in seed, leaf, and pod wall and their relationship to seed filling in soybeans. Crop Pasture Sci 61:103–110

    Article  CAS  Google Scholar 

  • Ljung K, Hull AK, Kowalczyk M, Marchant A, Celenza J, Cohen JD, Sandberg G (2002) Biosynthesis, conjugation, catabolism and homeostasis of indole-3-acetic acid in Arabidopsis thaliana. Plant Mol Biol 49:249–272

    Article  PubMed  CAS  Google Scholar 

  • Ludwig-Muller J (2011) Auxin conjugates: their role for plant development and in the evolution of land plants. J Exp Bot 62:1757–1773

    Article  PubMed  Google Scholar 

  • Lulsdorf MM, Yuan HY, Slater SMH, Vandenberg A, Han X, Zaharia LI, Abrams SR (2013) Endogenous hormone profiles during early seed development of C. arietinum and C. anatolicum. Plant Growth Regul. http://www.springerlink.com/openurl.asp?genre=article&id=doi:10.1007/s10725-013-9819-2

  • Magnus V, Ozga JA, Reinecke DM, Pierson GL, Larue TA, Cohen JD, Brenner ML (1997) 4-Chloroindole-3-acetic acid and indole-3-acetic acid in Pisum sativum. Phytochemistry 46:675–681

    Article  CAS  Google Scholar 

  • Menendez V, Revilla MA, Fal MA, Fernandez H (2009) The effect of cytokinins on growth and sexual organ development in the gametophyte of Blechnum spicant L. Plant Cell Tiss Organ Cult 96:245–250

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Nadeau CD, Ozga JA, Kurepin LV, Jin A, Pharis RP, Reinecke DM (2011) Tissue-specific regulation of gibberellin biosynthesis in developing pea seeds. Plant Physiol 156:897–912

    Article  PubMed  CAS  Google Scholar 

  • Nambara E, Marion-Poll A (2003) ABA action and interactions in seeds. Trends Plant Sci 8:213–217

    Article  PubMed  CAS  Google Scholar 

  • Oetiker JH, Aeschbacher G (1997) Temperature-sensitive plant cells with shunted indole-3-acetic acid conjugation. Plant Physiol 114:1385–1395

    PubMed  CAS  Google Scholar 

  • Ostrowski M, Jakubowska A (2011) Purification and biochemical characterization of indole-3-acetyl-aspartic acid synthetase from immature seeds of pea (Pisum sativum). J Plant Growth Regul 30:30–40

    Article  CAS  Google Scholar 

  • Ozga JA, Reinecke DM, Ayele BT, Ngo P, Nadeau C, Wickramarathna AD (2009) Developmental and hormonal regulation of gibberellin biosynthesis and catabolism in pea fruit. Plant Physiol 150:448–462

    Article  PubMed  CAS  Google Scholar 

  • Park S, Ozga JA, Cohen JD, Reinecke DM (2010) Evidence of 4-Cl-IAA and IAA bound to proteins in pea fruit and seeds. J Plant Growth Regul 29:184–193

    Article  CAS  Google Scholar 

  • Pinto DLP, de Almeida AMR, Rego MM, da Silva ML, de Oliveira EJ, Otoni WC (2011) Somatic embryogenesis from mature zygotic embryos of commercial passionfruit (Passiflora edulis Sims) genotypes. Plant Cell Tiss Organ Cult 107:521–530

    Article  Google Scholar 

  • Powell AF, Paleczny AR, Olechowski H, Emery RJ (2013) Changes in cytokinin form and concentration in developing kernels correspond with variation in yield among field-grown cultivars. Plant Physiol Biochem 64:33–40

    Article  PubMed  CAS  Google Scholar 

  • Quesnelle PE, Emery RJN (2007) cis-Cytokinins that predominate in Pisum sativum during early embryogenesis will accelerate embryo growth in vitro. Can J Bot 85:91–103

    Article  Google Scholar 

  • Reinecke D (1999) 4-Chloroindole-3-acetic acid and plant growth. Plant Growth Reg 27:3–13

    Article  CAS  Google Scholar 

  • Reinecke DM, Ozga JA, Magnus V (1995) Effect of halogen substitution of indole-3-acetic acid on biological activity in pea fruit. Phytochemistry 40:1361–1366

    Article  CAS  Google Scholar 

  • Rijavec T, Jain M, Dermastia M, Chourey PS (2011) Spatial and temporal profiles of cytokinin biosynthesis and accumulation in developing caryopses of maize. Ann Bot 107:1235–1245

    Article  PubMed  CAS  Google Scholar 

  • Rodrigo MJ, Garcia-Martinez JL, Santes CM, Gaskin P, Hedden P (1997) The role of gibberellins A1 and A3 in fruit growth of Pisum sativum L. and the identification of gibberellins A4 and A7 in young seeds. Planta 201:446–455

    Article  CAS  Google Scholar 

  • Rosquete MR, Barbez E, Kleine-Vehn J (2012) Cellular auxin homeostasis: gatekeeping is housekeeping. Mol Plant 5:772–786

    Article  PubMed  Google Scholar 

  • Sakakibara H (2006) Cytokinins: activity biosynthesis, and translocation. Annu Rev Plant Biol 57:431–449

    Article  PubMed  CAS  Google Scholar 

  • Sasaki K, Shimomura K, Kamada H, Harada H (1994) IAA metabolism in embryogenic and non-embryogenic carrot cells. Plant Cell Physiol 35:1159–1164

    CAS  Google Scholar 

  • Simon S, Petrasek J (2011) Why plants need more than one type of auxin. Plant Sci 180:454–460

    Article  PubMed  CAS  Google Scholar 

  • Singh DP, Filardo FF, Storey R, Jermakow AM, Yamajuchi S, Swain SM (2010) Overexpression of a gibberellin inactivation gene alters seed development, KNOX gene expression, and plant development in Arabidopsis. Physiol Plant 138:74–90

    Article  PubMed  CAS  Google Scholar 

  • Steele KP, Wojciechowski MF (2003) Phylogenetic analyses of tribes Trifolieae and Vicieae, based on sequences of the plastid gene, matK (Papilionoideae: Leguminosae). In: Klitgaard BB, Bruneau A (eds) Advances in legume systematic, part 10, higher level systematics. Royal Botanic Gardens, Kew, pp 355–370

    Google Scholar 

  • Swain SM, Singh DP (2005) Tall tales from sly dwarves: novel functions of gibberellins in plant development. Trends Plant Sci 10:123–129

    Google Scholar 

  • Tam YY, Epstein E, Normanly J (2000) Characterization of auxin conjugates in Arabidopsis. Low steady-state levels of indole-3-acetyl-aspartate, indole-3-acetyl-glutamate, and indole-3-acetyl-glucose. Plant Physiol 123:589–595

    Article  PubMed  CAS  Google Scholar 

  • Teale WD, Paponov IA, Palme K (2006) Auxin in action: signalling, transport and the control of plant growth and development. Nat Rev Mol Cell Biol 7:847–859

    Article  PubMed  CAS  Google Scholar 

  • Toker C, Ulger S, Karhan M, Canci H, Akdesir O, Ertoy N, Cagirgan MI (2005) Comparison of some endogenous hormone levels in different parts of chickpea (Cicer arietinum L.). Genet Resour Crop Evol 52:233–237

    Article  CAS  Google Scholar 

  • Toker C, Ulger S, Cagirgan MI (2006) Endogenous hormone variations in annual wild Cicer species. Genet Resour Crop Evol 53:171–177

    Article  CAS  Google Scholar 

  • Van Daele I, Gonzalez N, Vercautern I, de Smet L, Inze D, Roldan-Ruiz I, Vuylsteke M (2010) A comparative study of seed yield parameters in Arabidopsis thaliana mutants and transgenics. Plant Biotechnol J 10:488–500

    Article  Google Scholar 

  • Weber H, Borisjuk L, Wobus U (2005) Molecular physiology of legume seed development. Annu Rev Plant Biol 56:253–279

    Article  PubMed  CAS  Google Scholar 

  • Yamaguchi S (2008) Gibberellin metabolism and its regulation. Annu Rev Plant Biol 59:225–251

    Article  PubMed  CAS  Google Scholar 

  • Zaharia LI, Galka MM, Ambrose SJ, Abrams SR (2005) Preparation of deuterated abscisic acid metabolites for use in mass spectrometry and feeding studies. J Label Cmpd Radiopharm 48:435–445

    Article  CAS  Google Scholar 

  • Zeevaart JAD (2003) Regulators of growth: abscisic acid. In: Thomas B (ed) Encyclopedia of applied plant sciences. Elsevier Ltd, Oxford, pp 995–999

Download references

Acknowledgments

Financial support for this project was provided by the Saskatchewan Agricultural Development Fund and Saskatchewan Pulse Growers. We acknowledge technical assistance from T. Ament, K. Arsenault, S.B. Mudiyanselage, V. Cekic, and M. Lafond.

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Authors and Affiliations

  1. Crop Development Centre (CDC), University of Saskatchewan, 51 Campus Drive, Saskatoon, SK S7N 5A8, Canada

    Susan M. H. Slater, Hai Ying Yuan, Monika M. Lulsdorf & Albert Vandenberg

  2. National Research Council of Canada-Saskatoon (NRCC-SK), 110 Gymnasium Place, Saskatoon, SK S7N 0W9, Canada

    L. Irina Zaharia & Xiumei Han

  3. Saskatchewan Structural Sciences Centre, University of Saskatchewan, 110 Science Place, Saskatoon, SK S7N 5C7, Canada

    Suzanne R. Abrams

Authors
  1. Susan M. H. Slater
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  2. Hai Ying Yuan
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  3. Monika M. Lulsdorf
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  4. Albert Vandenberg
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  5. L. Irina Zaharia
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  6. Xiumei Han
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  7. Suzanne R. Abrams
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Correspondence to Susan M. H. Slater.

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Communicated by P. Kumar.

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Slater, S.M.H., Yuan, H.Y., Lulsdorf, M.M. et al. Comprehensive hormone profiling of the developing seeds of four grain legumes. Plant Cell Rep 32, 1939–1952 (2013). https://doi.org/10.1007/s00299-013-1505-3

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  • DOI: https://doi.org/10.1007/s00299-013-1505-3

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