Skip to main content

The evolution of the plant genome-to-morphology auxin circuit

Theory in Biosciences volume 135, pages 175–186 (2016)Cite this article

Abstract

In his Generelle Morphologie der Organismen (1866), 150 years ago, Ernst Haeckel (1834–1919) combined developmental patterns in animals with the concept of organismic evolution, and 50 years ago, a new era of plant research started when focus shifted from crop species (sunflower, maize etc.) to thale cress (Arabidopsis thaliana) as a model organism. In this contribution, we outline the general principles of developmental evolutionary biology sensu Haeckel and describe the evolutionary genome-to-morphology-plant hormone auxin (IAA, indole-3-acetic acid)-circuit with reference to other phytohormones and a focus on land plants (embryophytes) plus associated epiphytic microbes. Our primary conclusion is that a system-wide approach is required to truly understand the ontogeny of any organism, because development proceeds according to signal pathways that integrate and respond to external as well as internal stimuli. We also discuss IAA-regulated embryology in A. thaliana and epigenetic phenomena in the gametophyte development, and outline how these processes are connected to the seminal work of Ernst Haeckel.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

Price includes VAT (USA)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  • Bartel B (1997) Auxin biosynthesis. Annu Rev Plant Physiol Plant Mol Biol 48:51–66

    CAS  Article  PubMed  Google Scholar 

  • Breidbach O (1998) Monismus um 1900—Wissenschaftspraxis oder Weltanschauung? Stapfia 56:289–316

    Google Scholar 

  • Chandler JW (2016) Auxin response factors. Plant Cell Environ 39:1014–1028

    CAS  Article  PubMed  Google Scholar 

  • Cheng Y, Dai X, Zhao Y (2007) Auxin synthesized by the YUCCA flavin monooxygenases is essential for embryogenesis and leaf formation in Arabidopsis. Plant Cell 19:2430–2439

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Cooke TJ, Poli D, Sztein AE, Cohen JD (2002) Evolutionary patterns in auxin action. Plant Mol Biol 49:319–338

    CAS  Article  PubMed  Google Scholar 

  • Darwin C (1859) On the origin of species by means of natural selection, or the preservation of favoured races in the struggle for life. John Murray, London

    Book  Google Scholar 

  • Darwin C (1860) Über die Entstehung der Arten im Thier- und Pflanzenreich durch natürliche Züchtung oder Erhaltung der vervollkommneten Rassen im Kampfe um’s Daseyn (translated by H. G. Bronn). E. Schweizerbart’sche Verlagshandlung und Druckerei, Stuttgart

  • Darwin C (1862) On the various contrivances by which British and foreign orchids are fertilized by insects, and on the good effects of intercrossing. John Murray, London

    Google Scholar 

  • De Smet I, Jürgens G (2007) Patterning the axis in plants—auxin in control. Curr Opin Genet Dev 17:337–343

    Article  PubMed  Google Scholar 

  • 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

    CAS  Article  PubMed  Google Scholar 

  • Duca D, Lorv J, Patten CL, Rose D, Glick BR (2014) Indole-3-acetic acid in plant–microbe interactions. Antonie Van Leeuwenhoek 106:85–125

    CAS  Article  PubMed  Google Scholar 

  • Feng M, Kim J-Y (2015) Revisiting apoplastic auxin signaling mediated by auxin binding protein 1. Mol Cell 38:829–835

    CAS  Article  Google Scholar 

  • Friml J, Vieten A, Sauer M, Weijers D, Schwarz H, Hamann T, Offringa R, Jügens G (2003) Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis. Nature 426:147–153

    CAS  Article  PubMed  Google Scholar 

  • Fujita T, Sakaguchi H, Hiwatashi Y, Wagstaff SJ, Ito M, Deguchi H, Sato T, Hasebe M (2008) Convergent evolution of shoots in land plants: lack of auxin polar transport in moss shoots. Evol Dev 10:176–186

    CAS  Article  PubMed  Google Scholar 

  • 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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Goodrich J (1998) Plant development: medea’s maternal instinct. Curr Biol 8:480–484

    Article  Google Scholar 

  • Grones P, Friml J (2015) Auxin transporters and binding proteins at a glance. J Cell Sci 128:1–7

    CAS  Article  PubMed  Google Scholar 

  • Haeckel E (1866) Generelle Morphologie der Organismen. Allgemeine Grundzüge der organischen Formen-Wissenschaft, mechanisch begründet durch die von Charles Darwin reformierte Descendenz-Theorie, vols I and II. Verlag Georg Reimer, Berlin

  • Haecker A, Gross-Hardt R, Geiges B, Sarkar A, Breuninger H, Herrmann M, Laux T (2004) Expression dynamics of WOX genes mark cell fate decisions during early embryonic patterning in Arabidopsis thaliana. Development 131:657–668

    CAS  Article  PubMed  Google Scholar 

  • Hartwig T, Wang Z-Y (2015) The molecular circuit of steroid signalling in plants. Essays Biochem 58:71–82

    Article  PubMed  Google Scholar 

  • Hayashi K, Tan X, Zheng N, Hatate T, Kimura Y, Kepinski S, Nozaki H (2008) Small-molecule agonists and antagonists of F-box protein-substrate interactions in auxin perception and signaling. Proc Natl Acad Sci USA 105:5632–5637

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Henschel K, Kofuji R, Hasebe M, Saedler H, Münster T, Theißen G (2002) Two ancient classes of MIKC-type MADS-box genes are present in the moss Physcomitrella patens. Mol Biol Evol 19:801–814

    CAS  Article  PubMed  Google Scholar 

  • Hornschuh M, Grotha R, Kutschera U (2006) Moss-associated methylobacteria as phytosymbionts: an experimental study. Naturwissenschaften 93:480–486

    CAS  Article  PubMed  Google Scholar 

  • Hossfeld U (2010) Ernst Haeckel. Orange Press, Freiburg

    Google Scholar 

  • Hossfeld U (2016) Geschichte der biologischen Anthropologie, 2nd edn. Franz Steiner Verlag, Stuttgart

    Google Scholar 

  • Hossfeld U, Olsson L (2003) The road from Haeckel: the Jena tradition in evolutionary morpohology and the origins of “Evo-Devo”. Biol Philos 18:285–307

    Article  Google Scholar 

  • Jin Q, Scherp P, Heimann K, Hasenstein KH (2007) Auxin and cytoskeletal organization in algae. Cell Biol Int 32:542–545

    Article  PubMed  Google Scholar 

  • Johri MM (2004) Possible origin of hormonal regulation in green plants. Proc Indian Nat Sci Acad B 70:335–465

    CAS  Google Scholar 

  • Johri MM (2008) Hormonal regulation in green plant lineage families. Physiol Mol Biol Plants 14:23–38

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Kim TW, Wang Z-Y (2010) Brassinosteroid signal transduction from receptor kinase to transcription factors. Annu Rev Plant Biol 61:681–704

    CAS  Article  PubMed  Google Scholar 

  • Klaembt D, Knauth B, Dittmann I (1992) Auxin dependent growth of rhizoids of Chara globularis. Physiol Plant 85:537–540

    CAS  Article  Google Scholar 

  • Kohler C, Hennig L, Bouveret R, Gheyselinck J, Grossniklaus U, Gruissem W (2003) Arabidopsis MSI1 is a component of the MEA/FIE Polycomb group complex and required for seed development. EMBO J 22:4804–4814

    Article  PubMed  PubMed Central  Google Scholar 

  • Koornneef M, Meinke D (2010) The development of Arabidopsis as a model plant. Plant J 61:909–921

    CAS  Article  PubMed  Google Scholar 

  • Kutschera U (2007) Plant-associated methylobacteria as co-evolved phytosymbionts: a hypothesis. Plant Signal Behav 2:74–78

    Article  PubMed  PubMed Central  Google Scholar 

  • Kutschera U, Briggs WR (2009) From Charles Darwin’s botanical country-house studies to modern plant biology. Plant Biol 11:785–795

    CAS  Article  PubMed  Google Scholar 

  • Kutschera U, Briggs WR (2013) Seedling development in buckwheat and the discovery of the photomorphogenic shade-avoidance response. Plant Biol 15:931–940

    CAS  Article  PubMed  Google Scholar 

  • Kutschera U, Briggs WR (2016) Phototropic solar tracking in sunflower plants: an integrative perspective. Ann Bot 117:1–8

    Article  PubMed  Google Scholar 

  • 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

    CAS  Article  PubMed  Google Scholar 

  • Kutschera U, Niklas KJ (2009) Evolutionary plant physiology: Charles Darwin’s forgotten synthesis. Naturwissenschaften 96:1339–1354

    CAS  Article  PubMed  Google Scholar 

  • Kutschera U, Wang Z-Y (2012) Brassinosteroid action in flowering plants: a Darwinian perspective. J Exp Bot 63:3511–3522

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Kutschera U, Wang Z-Y (2016) Growth-limiting proteins in maize coleoptiles and the auxin-brassinosteroid hypothesis of mesocotyl elongation. Protoplasma 253:3–14

    CAS  Article  PubMed  Google Scholar 

  • 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

    CAS  Article  PubMed  Google Scholar 

  • Lachner M, O’Sullivan RJ, Jenuwein T (2003) An epigenetic road map for histone lysine methylation. J Cell Sci 116:2117–2124

    CAS  Article  PubMed  Google Scholar 

  • Langdale JA (2008) Evolution of developmental mechanisms in plants. Curr Opin Genet Dev 18:368–373

    CAS  Article  PubMed  Google Scholar 

  • Lau S, Shao N, Bock R, Jürgens G, De Smet I (2009) Auxin signaling in algal lineages: fact or myth? Trends Plant Sci 14:1360–1385

    Article  Google Scholar 

  • Lau S, Slane D, Herud O, Kong J, Jürgens G (2012) Early embryogenesis in flowering plants: setting up the basic body pattern. Annu Rev Plant Biol 63:483–506

    CAS  Article  PubMed  Google Scholar 

  • Le Bail A, Billoud B, Kowalczyk N, Kowalczyk M, Gicquel M, Le Panse S, Stewart S, Scornet D, Cock JM, Ljung K, Charrier B (2010) Auxin metabolism and function in the multicellular brown alga Ectocarpus siliculosus. Plant Physiol 153:128–144

    Article  PubMed  PubMed Central  Google Scholar 

  • Liepman AH, Wightman R, Geshi N et al (2010) Arabidopsis—a powerful model system for plant cell wall research. Plant J 61:1107–1121

    CAS  Article  PubMed  Google Scholar 

  • Ludwig-Müller 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 

  • Mosquna A, Katz A, Decler EL, Rensing SA, Reski R, Ohad N (2009) Regulation of stem cell maintenance by the Polycomb protein FIE has been conserved during land plant evolution. Development 136:2433–2444

    CAS  Article  PubMed  Google Scholar 

  • Muto H, Watahiki M, Nakamoto D, Kinjo M, Yamamoto KT (2007) Specificity and similarity of functions of the Aux/IAA genes in auxin signaling of Arabidopsis revealed by promoter-exchange experiments among MSG2/IAA19, AXR2/IAA7, and SLR/IAA14. Plant Physiol 144:187–196

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Nekrasov M, Wild B, Muller J (2005) Nucleosome binding and histone methyltransferase activity of Drosophila PRC2. EMBO Rep 6:348–353

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Niklas KJ (1992) Plant biomechanics. The University of Chicago Press, Chicago

    Google Scholar 

  • Niklas KJ (1997) The evolutionary biology of plants. The University of Chicago Press, Chicago

    Google Scholar 

  • Niklas KJ (2004) The cell walls that bind the tree of life. Bioscience 54:841–851

    Article  Google Scholar 

  • Niklas KJ, Kutschera U (2009) The evolutionary development of plant body plans. Funct Plant Biol 36:682–695

    Article  Google Scholar 

  • Niklas KJ, Kutschera U (2010) The evolution of the land plant life cycle. New Phytol 185:27–41

    CAS  Article  PubMed  Google Scholar 

  • Niklas KJ, Kutschera U (2012) Plant development, auxin, and the subsystem incompleteness theorem. Front Plant Sci 3(37):1–11

    Google Scholar 

  • Niklas KJ, Cobb ED, Kutschera U (2014) Did meiosis evolve before sex and the evolution of eukaryotic life cycles? Bioessays 36:1091–1101

    Article  PubMed  Google Scholar 

  • Niklas KJ, Cobb ED, Kutschera U (2016) Haeckel’s biogenetic law and the land plant phylotypic stage. Bioscience 66:510–519

    Article  Google Scholar 

  • Paponov IA, Paponov MT, Teale W, Menges M, Chakrabortee S, Murray JAH, Palme K (2008) Comprehensive transcriptome analysis of auxin responses in Arabidopsis. Mol Plant 1:321–337

    CAS  Article  PubMed  Google Scholar 

  • Pils B, Heyl A (2009) Unraveling the evolution of cytokinin signaling. Plant Physiol 151:782–791

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Poli DB, Jacobs M, Cooke TJ (2003) Auxin regulation of axial growth in bryophyte sporophytes: its potential significance for the evolution of early land plants. Am J Bot 90:1405–1415

    CAS  Article  PubMed  Google Scholar 

  • Provart NJ, Alonso J, Assmann SM et al (2016) 50 years of Arabidopsis research: highlights and future directions. New Phytol 209:921–944

    CAS  Article  PubMed  Google Scholar 

  • Rensing SA (2016) (Why) does evolution favour embryogenesis? Trends Plant Sci (in press)

  • Rensing SA, Land D, Zimmer AD et al (2008) The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science 319:64–69

    CAS  Article  PubMed  Google Scholar 

  • Ross JJ, Reid JB (2010) Evolution of growth-promoting plant hormones. Funct Plant Biol 37:795–805

    CAS  Article  Google Scholar 

  • Shin R, Burch AY, Huppert KA, Tiwari SB, Murphy AS, Guilfoyle TJ, Schachtman DP (2007) The Arabidopsis transcription factor MYB77 modulates auxin signal transcription. Plant Cell 19:2440–2453

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Spaepen S, Vanderleyden J, Remans R (2007) Indole-3-acetic acid in micobial and microorganism-plant signaling. FEMS Microbiol Rev 31:425–448

    CAS  Article  PubMed  Google Scholar 

  • Tanabe Y, Hasebe M, Sekimoto H, Nishiyama T, Kitani M, Henschel K, Munster T, Theißen G, Nozaki H, Ito M (2005) Characterization of MADS-box genes in charophycean green algae and its implications for the evolution of MADS-box genes. Proc Natl Acad Sci USA 102:2436–2441

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Tanahashi T, Sumikawa N, Kato M, Hasebe M (2005) Diversification of gene function: homologs of the floral regulator FLO/LFY control the first zygotic division in the moss Physcomitrella patens. Development 132:1727–1736

    CAS  Article  PubMed  Google Scholar 

  • Tanimoto M, Jowett J, Stirnberg P, Rouse D, Leyser O (2007) pa1–1 partially suppresses gain-of-function mutations in Arabidopsis AXR3/IAA17. BMC Plant Biol 7:20

    Article  PubMed  PubMed Central  Google Scholar 

  • Tao Y, Ferrer J-L, Ljung K, Pojer F et al (2008) Rapid synthesis of auxin via a new tryptophan-dependent pathway is required for shade avoidance in plants. Cell 133:164–176

    CAS  Article  PubMed  PubMed Central  Google Scholar 

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

    CAS  Article  Google Scholar 

  • Vieten A, Sauer M, Brewer PB, Friml J (2007) Molecular and cellular aspects of auxin-transport-mediated development. Trends Plant Sci 12:160–168

    CAS  Article  PubMed  Google Scholar 

  • Wang B, Chu J, Yu T, Xu Q, Sun X, Yuan J, Xiong G, Wang G, Wang Y, Li J (2015) Tryptophan-independent auxin biosynthesis contributes to early embryogenesis in Arabidopsis. Proc Natl Acad Sci USA 112:4821–4826

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Weijers D, Schlereth A, Ehrismann JS, Schwank G, Kientz M, Jürgens G (2006) Auxin triggers transient local signaling for cell specification in Arabidopsis embryogenesis. Dev Cell Biol 10:265–270

    CAS  Google Scholar 

  • Woodward AW, Bartel B (2005) Auxin: regulation, action, and interaction. Ann Bot 95:707–735

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Yin X, Struik PC (2010) Modeling the crop: from systems dynamic to systems biology. J Exp Bot 61:2171–2183

    CAS  Article  PubMed  Google Scholar 

  • Zhao Y (2010) Auxin biosynthesis and its role in plant development. Annu Rev Plant Biol 61:49–64

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Zhao Y (2012) Auxin biosynthesis: a simple two-step pathway converts tryptophan to indole-3-acetic acid. Mol Plant 5:334–338

    CAS  Article  PubMed  Google Scholar 

Download references

Acknowledgments

The cooperation of the authors was supported by the Alexander von Humboldt-Stiftung (Bonn, Germany) (AvH-Fellowship Stanford 2014/15 to UK).

Author information

Authors and Affiliations

  1. Institute of Biology, University of Kassel, 34109, Kassel, Germany

    Ulrich Kutschera

  2. Plant Biology Section, School of Integrative Plant Science, Cornell University, Ithaca, NY, 14853, USA

    Karl J. Niklas

Authors
  1. Ulrich Kutschera
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Karl J. Niklas
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ulrich Kutschera.

Additional information

This article forms part of a special issue of Theory in Biosciences in commemoration of Olaf Breidbach.

Dedicated to the memory of Olaf Breidbach (1957–2014).

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Kutschera, U., Niklas, K.J. The evolution of the plant genome-to-morphology auxin circuit. Theory Biosci. 135, 175–186 (2016). https://doi.org/10.1007/s12064-016-0231-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12064-016-0231-0

Keywords

  • Auxin
  • Gene networks
  • IAA
  • Plant evolution
  • Transcription factors