The evolutionary development of plant body plans
Karl J. Niklas A C and Ulrich Kutschera BA Department of Plant Biology, Cornell University, Ithaca, NY 14853, USA.
B Institute of Biology, University of Kassel, Heinrich-Plett-Strasse 40, D-34109 Kassel, Germany.
C Corresponding author. Email: kjn2@cornell.edu
This paper is part of an ongoing series: ‘The Evolution of Plant Functions’.
Functional Plant Biology 36(8) 682-695 https://doi.org/10.1071/FP09107
Submitted: 12 May 2009 Accepted: 12 June 2009 Published: 23 July 2009
Abstract
Evolutionary developmental biology, cladistic analyses, and paleontological insights make it increasingly clear that regulatory mechanisms operating during embryogenesis and early maturation tend to be highly conserved over great evolutionary time scales, which can account for the conservative nature of the body plans in the major plant and animal clades. At issue is whether morphological convergences in body plans among evolutionarily divergent lineages are the result of adaptive convergence or ‘genome recall’ and ‘process orthology’. The body plans of multicellular photosynthetic eukaryotes (‘plants’) are reviewed, some of their important developmental/physiological regulatory mechanisms discussed, and the evidence that some of these mechanisms are phyletically ancient examined. We conclude that endosymbiotic lateral gene transfers, gene duplication and functional divergence, and the co-option of ancient gene networks were key to the evolutionary divergence of plant lineages.
Additional keywords: apogamy, apospory, auxin, endosymbiosis, euphyllophytes, floral identity genes, homeodomain genes, MADS-box genes, plant evolution, TIR1.
Archibald JM
(2009) Green evolution, green revolution. Science 324, 191–192.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Aso K,
Kato M,
Banks JA, Hasebe M
(1999) Characterization of homeodomain-leucine zipper genes in the fern Ceratopteris richardii and the evolution of the homeodomain-leucine zipper gene family in vascular plants. Molecular Biology and Evolution 16, 544–552.
| PubMed |
Axtell MJ,
Snyder JA, Bartel DP
(2007) Common functions for diverse small RNAs of land plants. The Plant Cell 19, 1750–1769.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Bayer M,
Nawy T,
Giglione C,
Galli M,
Meinnel T, Lukowitz W
(2009) Paternal control of embryonic patterning in Arabidopsis thaliana. Science 323, 1485–1488.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Beerling DJ
(2005) Leaf evolution: gases, genes and geochemistry. Annals of Botany 96, 345–352.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Beerling DJ, Fleming AJ
(2007) Zimmermann’s telome theory of megaphyll leaf evolution: a molecular and cellular critique. Current Opinion in Plant Biology 10, 4–12.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Bhattacharya D, Medlin L
(1995) The phylogeny of plastids: a review based on comparisons of small-subunit ribosomal RNA coding regions. Journal of Phycology 31, 489–498.
| Crossref | GoogleScholarGoogle Scholar |
Chen J-G,
Shimomura S,
Sitbon F,
Sandberg G, Jones AM
(2001) The role of auxin-binding protein 1 in the expansion of tobacco cell. The Plant Journal 28, 607–617.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Crepet WL, Niklas KJ
(2009) Darwin’s second “abominable mystery”: why are there so many angiosperms? American Journal of Botany 96, 366–381.
| Crossref | GoogleScholarGoogle Scholar |
Delmer DP
(1999) Cellulose biosynthesis: exciting times for a difficult field. Annual Review of Plant Physiology and Plant Molecular Biology 50, 245–276.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Dharmasiri N,
Dharmasiri S, Estelle M
(2005) The F-box protein TIR1 is an auxin receptor. Nature 435, 441–445.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Doebley J
(2004) The genetics of maize evolution. Annual Review of Genetics 38, 37–59.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Flores E,
Herrera A,
Wolk CP, Maldener I
(2006) Is the periplasm continuous in filamentous multicellular cyanobacteria. Trends in Microbiology 14, 439–443.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Floyd SK, Bowman JL
(2006) Distinct developmental mechanisms reflect the independent origins of leaves in vascular plants. Current Biology 16, 1911–1917.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Friml J,
Vieten A,
Sauer M,
Weijers D,
Schwarz H,
Hamann T,
Offringa R, Jürgens G
(2003) Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis. Nature 426, 147–153.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Fryer G
(1999) The case of the one-eyed shrimp: are ancient atavisms possible? Journal of Natural History 33, 791–798.
| Crossref | GoogleScholarGoogle 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. Evolution & Development 10, 176–186.
| PubMed |
Geldner N
(2009) Cell polarity in plants – a PARspective on PINs. Current Opinion in Plant Biology 12, 42–48.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Gerrienne P,
Dilcher DL,
Bergamaschi S,
Milagres I,
Pereira E, Rodrigues MAC
(2006) An exceptional specimen of the early land plant Cooksonia paranensis, and a hypothesis on the life cycle of the earliest eutracheophytes. Review of Palaeobotany and Palynology 142, 123–130.
| Crossref | GoogleScholarGoogle Scholar |
Halder G,
Callaerts P, Gehring WJ
(1995) Induction of ectopic eyes by targeted expression of the eyeless gene in Drosophila. Science 267, 1788–1792.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Harrison CJ,
Corley SB,
Moylen EC,
Alexander DL,
Scotland RW, Langdale JA
(2005) Independent recruitment of a conserved developmental mechanism during leaf evolution. Nature 434, 509–514.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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. Molecular Biology and Evolution 19, 801–814.
| PubMed |
Johri MM
(2004) Possible origin of hormonal regulation in green plants. Proceedings of the Indian National Science Academy Part B Biological Sciences 70, 335–365.
Johri MM
(2008) Hormonal regulation in green plant lineage families. Physiology and Molecular Biology of Plants 14, 23–38.
| Crossref | GoogleScholarGoogle Scholar |
Kenrick P, Crane PR
(1997a) The origin and early evolution of plants on land. Nature 389, 33–39.
| Crossref | GoogleScholarGoogle Scholar |
Kerp H,
Trewin NH, Hass H
(2004) Rhynie Chert gametophytes. Transactions of the Royal Society of Edinburgh. Earth Sciences 94, 411–428.
Kerstetter RA,
Bollman K,
Taylor RA,
Bombles K, Poethig RS
(2001)
KANADI regulates organ polarity in Arabidopsis. Nature 411, 706–709.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kutschera U
(2003) Auxin-induced cell elongation in grass coleoptiles: a phytohormone in action. Current Topics in Plant Biology 4, 27–46.
Kutschera U
(2006) Acid growth and plant development. Science 311, 952–954.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kutschera U
(2008) The outer epidermal wall: design and physiological role of a composite structure. Annals of Botany 101, 615–621.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kutschera U, Edelmann HG
(2005) Osmiophilic nanoparticles in epidermal cells of grass coleoptiles: implications for growth and gravitropism. Recent Research Developments in Plant Science 3, 1–14.
Kutschera U, Niklas KJ
(2004) The modern theory of biological evolution: an expanded synthesis. Naturwissenschaften 91, 255–276.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kutschera U, Niklas KJ
(2005) Endosymbiosis, cell evolution, and speciation. Theory in Biosciences 124, 1–24.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kutschera U, Niklas KJ
(2008) Macroevolution via secondary endosymbiosis: a Neo-Goldschmidtian view of unicellular hopeful monsters and Darwin’s primordial intermediate form. Theory in Biosciences 127, 277–289.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Lee JH,
Lin HW,
Joo S, Goodenough U
(2008) Early sexual origins of homeodomain heterodimerization and evolution of the plant KNOX/BELL family. Cell 133, 829–840.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Li Y,
Hagen G, Guilfoyle TJ
(1992) Altered morphology in transgenic tobacco plants that overproduce cytokinins in specific tissues and organs. Developmental Biology 153, 386–395.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Long JA,
Ohio C,
Smith ZR, Meyerowitz EM
(2006)
TOPLESS regulates apical embryonic fate in Arabidopsis. Science 312, 1520–1523.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Maizel A,
Busch MA,
Tanahashi T,
Perkovic J,
Kato M,
Hasebe M, Weigel D
(2005) The floral regulator LEAFY evolves by substitutions in the DNA binding domain. Science 308, 260–263.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Marshall CR,
Raff EC, Raff RA
(1994) Dollo’s law and the death and resurrection of genes. Proceedings of the National Academy of Sciences of the United States of America 91, 12283–12287.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
McConnell J,
Emery J,
Eshed Y,
Bao N,
Bowman J, Barton MK
(2001)
PHABULOSA and PHAVOLUTA in determining radial patterning in shoots. Nature 411, 709–713.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Muday GK, DeLong A
(2001) Polar auxin transport: controlling where and how much. Trends in Plant Science 6, 535–542.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Niklas KJ
(2000) The evolution of plant body plans – a biomechanical perspective. Annals of Botany 85, 411–438.
| Crossref | GoogleScholarGoogle Scholar |
Niklas KJ
(2004) The cell walls that bind the tree of life. Bioscience 54, 831–841.
| Crossref | GoogleScholarGoogle Scholar |
Nobles DR,
Romanovicz DK, Brown RM
(2001) Cellulose in cyanobacteria. Origin of vascular plant cellulose synthase? Plant Physiology 127, 529–542.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Palme K,
Hesse T,
Campos N,
Garbers C,
Yanofsky MF, Schell J
(1992) Molecular analyses of an auxin binding protein gene located on chromosome 4 of Arabidopsis. The Plant Cell 4, 193–201.
| Crossref |
PubMed |
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. American Journal of Botany 90, 1405–1415.
| Crossref | GoogleScholarGoogle Scholar |
Ratcliffe OJ,
Riechman JL, Zhang JZ
(2000)
INTERFASCICULAR FIBERLESS1 is the same gene as REVOLUTA. The Plant Cell 12, 315–317.
| Crossref |
PubMed |
Raven J
(1997) Multiple origins of plasmodesmata. European Journal of Phycology 32, 95–101.
| Crossref | GoogleScholarGoogle Scholar |
Richmond TA, Somerville CR
(2000) The cellulose synthase superfamily. Plant Physiology 124, 495–498.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Roberts AW,
Roberts EM, Delmer DP
(2002) Cellulose synthase (CesA) genes in the green alga Mesotaenium caldariorum. Eukaryotic Cell 1, 847–855.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Römling U
(2002) Molecular biology of cellulose production in bacteria. Research in Microbiology 153, 205–212.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Ruegger M,
Dewey E,
Gray WM,
Hobbie L,
Turner J, Estelle M
(1998) The TIR1 protein of Arabidopsis functions in auxin response and is related to human SKP2 and yeast Grr1p. Genes & Development 12, 198–207.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Sakakibara K,
Nishiyama T,
Kato M, Hasebe M
(2001) Isolation of homeodomain-leucine zipper genes from the moss Physcomitrella patens and the evolution of homeodomain-leucine zipper genes in land plants. Molecular Biology and Evolution 18, 491–502.
| PubMed |
Sakakibara K,
Nishiyama T,
Deguchi H, Hasebe M
(2008) Class 1 KNOX genes are not involved in shoot development in the moss Physcomitrella patens but do function in sporophyte development. Evolution & Development 10, 555–566.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Scherp P,
Grotha R, Kutschera U
(2001) Occurrence and phylogenetic significance of cytokinesis-related callose in green algae, bryophytes, ferns an seed plants. Plant Cell Reports 20, 143–149.
| Crossref | GoogleScholarGoogle Scholar |
Soltis PS,
Brochington SF,
Yoo M-Y,
Piedrahita A,
Latvis M,
Moore MJ,
Chanderbali AS, Soltis DE
(2009) Floral variation and floral genetics in basal angiosperms. American Journal of Botany 96, 110–128.
| Crossref | GoogleScholarGoogle Scholar |
Steemans P,
Le Hérissé A,
Melvin J,
Miller MA,
Paris F,
Verniers J, Wellmann CH
(2009) Origin and radiation of the earliest vascular land plants. Science 324, 353.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Sztein AE,
Cohan JD,
Slovin JP, Cooke TJ
(1995) Auxin metabolism in representative land plants. American Journal of Botany 82, 1514–1521.
| Crossref | GoogleScholarGoogle 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 implication for the evolution of MADS-box genes. Proceedings of the National Academy of Sciences of the United States of America 102, 2436–2441.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Vergara CE, Carpita NC
(2001) β-D-glycan synthases and the CesA gene family: lessons to be learned from the mixed-linkage (1–3), (1–4) β-D-glucan synthase. Plant Molecular Biology 47, 145–160.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Winter K-U,
Becker A,
Münster T,
Kim JT,
Saedler H, Theißen G
(1999) MADS-box genes reveal that gnetophytes are more closely related to conifers than to flowering plants. Proceedings of the National Academy of Sciences of the United States of America 96, 7342–7347.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Worden AZ,
Lee J-H,
Mock T,
Rouzé P, Simmons MP ,
et al
.
(2009) Green evolution and dynamic adaptations revealed by the genomes of the marine picoeukaryotes Micromonas. Science 324, 268–272.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Zhong R, Ye ZH
(1999)
IFL1, a gene regulating interfascicular fibre differentiation in Arabidopsis, encodes a homeodomain-leucine zipper protein. The Plant Cell 11, 2139–2152.
| Crossref |
PubMed |
Zimmermann W
(1952) Main results of the telome theory. The Paleobotanist 1, 456–470.
