Model Plants for Understanding Evolution

Abstract

Plants are a hugely diverse group of organisms, including both land plants and aquatic algae, which inhabit a wide range of ecological niches across the planet. All plants arose from a single common ancestor and underwent a diversification that has shaped the earth's atmosphere and climate. One of the most important evolutionary transitions in the earth's history was the transition of plants to land. To understand how plants have evolved to possess such diversity of form, function and habitat requires in‐depth knowledge and comparison of plant development and physiology from a wide range of representative species. There are several key ‘traditional’ model organisms that have helped us understand plant evolution to date. However, there are significant gaps in our knowledge due to under‐representation in some parts of the green phylogenetic tree. The time is right to start filling these gaps using new and ‘up‐and‐coming’ green model organisms.

Key Concepts

  • Plants are a very diverse group of organisms that include both aquatic algae and land plants.
  • Land plants arose nearly half a billion years ago, while flowering plants arose more recently.
  • Model organisms are assumed to be representative of the biology of a larger group of organisms e.g. eukaryotes, plants and flowering plants.
  • Most plant model organisms are currently land plants, in particular flowering plants.
  • To understand plant evolution, we need better representation by model organisms within algae and non‐flowering plants.
  • With advances in genome sequencing, the challenge is now to find the most experimentally tractable plants to become new model organisms.

Keywords: land plants; algae; evolution; development; physiology

Figure 1. Simplified overview of Archeplastida, or plants. An ancestral eukaryotic cell engulfed a cyanobacterium approximately 1.6 billion years ago and gave rise to several lineages. The earliest evolving lineage was likely the Glaucophyta, a group of relatively uncommon unicellular freshwater algae. The Rhodophyta (red algae) were also early evolving, and are largely marine multicellular organisms. Green plants, or Viridiplantae, are composed of two clades, the Chlorophyta (comprising several groups of mainly marine algae) and the Streptophyta, namely Charophytes (largely freshwater algae) and the land plants. The land plants, from where most of our ‘green’ model organisms currently come, make up only one branch of the greater plant lineage. Based on Leliaert et al. (). Numbers of completely sequenced (published) genomes to date in each lineage are shown.
Figure 2. Schematic representation of land plant phylogeny with representative species. The earliest evolving land plants around 470 million years ago (MYA) were the bryophytes, small nonvascular plants falling into three groups: liverworts, mosses and hornworts. The earliest evolving vascular plants were lycophytes, followed by ferns. Evolution of the seed plants (spermatophytes) gave rise to gymnosperms and then angiosperms: the monocots and dicots diverged around 150 MYA. Images from top to bottom: the liverwort Marchantia polymorpha(Image from Younousse Saidi); the model moss Physcomitrella patens(Image from Younousse Saidi); the hornwort Anthoceros agrestis(Image from Eftychios Frangedakis); the lycophyte Selaginella kraussiana(Image from Younousse Saidi); a sporophyte of the emerging model fern Ceratopteris richardtii(Image from Andrew Plackett); the gymnosperm Araucaria araucana (monkey puzzle, a conifer, Image from Sue Bradshaw); the model monocot flowering plant Oryza sativa (rice, a grass, Image from Eugenio Sanchez‐Moran); the model dicot flowering plant Arabidopsis thaliana (mouse ear cress, Image from Eugenio Sanchez‐Moran). Numbers of sequenced genomes in each lineage are shown.
Figure 3. The model moss Physcomitrella patens. (a) Leafy haploid gametophyte plant bearing a mature diploid sporophyte (brown) containing haploid spores. (b) Protonemal, filamentous tissues growing in sterile culture on a petri dish. (c) Large sterile liquid culture of Physcomitrella tissue growing in a bioreactor. (d) Transgenic leafy Physcomitrella tissue expressing green fluorescent protein in both the nucleus and the cytosol. Images from Younousse Saidi.
Figure 4. Some emerging model plant systems. (a) The green alga Ulva mutabilis slender mutant, a naturally occurring mutant, ideal as a model organism (Wichard et al.,). Image from Ralf Kessler and Thomas Wichard. (b) Ectocarpus siliculosus, a brown alga from a separate eukaryotic lineage to plants, but sharing morphological and adaptive characteristics with red and green algae. Image from Benedicte Charrier. (c) A dissected leaf of Cardemine hirsuta(Images from Angela Hay) compared to (d) single leaf of Arabidopsis thaliana. Scale bars, 0.5 cm. Images from Angela Hay.
close

References

Alonso JM, Stepanova AN, Leisse TJ, et al. (2003) Genome‐wide insertional mutagenesis of Arabidopsis thaliana. Science 301: 653–657.

Aya K, Hiwatashi Y, Kojima M, et al. (2011) The Gibberellin perception system evolved to regulate a pre‐existing GAMYB‐mediated system during land plant evolution. Nature Communications 2: 544.

Bogaert KA, Arun A, Coehlo SM, et al. (2013) Brown algae as a model for plant organogenesis. Methods in Molecular Biology 959: 97–125.

Brouwer P, Bräutigam A, Külahoglu C, et al. (2014) Azolla domestication towards a biobased economy? New Phytologist 202: 1069–1082.

Canales C, Barkoulas M, Galinha C, et al. (2010) Weeds of change: cardamine hirsuta as a new model system for studying dissected leaf development. Journal of Plant Research 123: 25–33.

Clark J, Hidalgo O, Pellicer J, et al. (2016) Genome evolution of ferns: evidence for relative stasis of genome size across the fern phylogeny. New Phytologist 210: 1072–1082.

Cronk QC (2005) Plant eco‐devo: the potential of poplar as a model organism. New Phytologist 166: 39–48.

Delwiche CF and Cooper ED (2015) The evolutionary origin of a Terrestrial Flora. Current Biology 25: R899–R910.

Eckardt NA (2010) The Chlorella genome: big surprises from a small package. Plant Cell 22: 2924.

García‐Jiménez P and Robaina RR (2015) On reproduction in red algae: further research needed at the molecular level. Frontiers in Plant Science 6: 93.

Girin T, David LC, Chardin C, et al. (2014) Brachypodium: a promising hub between model species and cereals. Journal of Experimental Botany 65: 5683–5696.

Gupta BP and Sternberg PW (2003) The draft genome sequence of the nematode Caenorhabditis briggsae, a companion to C. elegans. Genome Biology 4: 238.

Harris EH (2001) Chlamydomonas as a model organism. Annual Review of Plant Physiology and Plant Molecular Biology 52: 363–406.

Hay A and Tsiantis M (2006) The genetic basis for differences in leaf form between Arabidopsis thaliana and its wild relative Cardamine hirsuta. Nature Genetics 38: 942–947.

Hay AS, Pieper B, Cooke E, et al. (2014) Cardamine hirsuta: a versatile genetic system for comparative studies. Plant Journal 78: 1–15.

Holtzman S, Miller D, Eisman R, et al. (2010) Transgenic tools for members of the genus Drosophila with sequenced genomes. Fly (Austin) 4: 349–362.

Hu TT, Pattyn P, Bakker EG, et al. (2011) The Arabidopsis lyrata genome sequence and the basis of rapid genome size change. Nature Genetics 43: 476–481.

Huang S, Weigel D, Beachy RN, et al. (2016) A proposed regulatory framework for genome‐edited crops. Nature Genetics 48: 109–111.

Ishizaki K, Nishihama R, Yamata KT, et al. (2015) Molecular genetic tools and techniques for Marchantia polymorpha research. Plant Cell Physiology 57 (2): 262–270.

Ji Q, Xu X and Wang K (2013) Genetic transformation of major cereal crops. International Journal of Developmental Biology 57: 495–508.

Kamath RS, Fraser AG, Dong Y, et al. (2003) Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 421: 231–237.

Keeling PJ (2010) The endosymbiotic origin, diversification and fate of plastids. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences 365: 729–748.

Khandelwal A, Cho SH, Marella H, et al. (2010) Role of ABA and ABI3 in desiccation tolerance. Science 327: 546.

Kirk DL (2004) Volvox. Current Biology 14: R599–R600.

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

Leliaert F, Smith DR, Moreau H, et al. (2012) Phylogeny and molecular evolution of the green algae. Critical Reviews in Plant Sciences 31: 1–46.

Li FW and Pryer KM (2014) Crowdfunding the Azolla fern genome project: a grassroots approach. GigaScience 3: 16.

Lin Z, Eaves DJ, Sanchez‐Moran E, et al. (2015) The Papaver rhoeas S determinants confer self‐incompatibility to Arabidopsis thaliana in planta. Science 350: 684–687.

Meyerowitz EM (2001) Prehistory and history of Arabidopsis research. Plant Physiology 125: 15–19.

Mikami K (2014) A technical breakthrough close at hand: feasible approaches toward establishing a gene‐targeting genetic transformation system in seaweeds. Frontiers in Plant Science 5: 498.

Nesi N, Delourme R, Brégeon M, et al. (2008) Genetic and molecular approaches to improve nutritional value of Brassica napus L. seed. Comptes Rendus Biologies 331: 763–771.

Peng J, Richards DE, Hartley NM, et al. (1999) ‘Green revolution’ genes encode mutant gibberellin response modulators. Nature 400: 256–261.

Pires ND, Yi K, Breuninger H, et al. (2013) Recruitment and remodeling of an ancient gene regulatory network during land plant evolution. Proceedings of the National Academy of Sciences of the United States of America 110: 9571–9576.

Prigge MJ and Bezanilla M (2010) Evolutionary crossroads in developmental biology: Physcomitrella patens. Development 137: 3535–3543.

Prochnik SE, Umen J, Nedelcu AM, et al. (2010) Genomic analysis of organismal complexity in the multicellular green alga Volvox carteri. Science 329: 223–226.

Proust H, Honkanen S, Jones VA, et al. (2016) RSL class I genes controlled the development of epidermal structures in the common ancestor of land plants. Current Biology 26: 93–99.

Qiu YL and Yu J (2003) Azolla – a model organism for plant genomic studies. Genomics, Proteomics & Bioinformatics 1: 15–25.

Sanders HL and Langdale JA (2013) Conserved transport mechanisms but distinct auxin responses govern shoot patterning in Selaginella kraussiana. New Phytologist 198: 419–428.

Sessa EB, Banks JA, Barker MS, et al. (2014) Between two fern genomes. GigaScience 3: 15.

Shoemaker DD, Lashkari DA, Morris D, et al. (1996) Quantitative phenotypic analysis of yeast deletion mutants using a highly parallel molecular bar‐coding strategy. Nature Genetics 14: 450–456.

Tougane K, Komatsu K, Bhyan SB, et al. (2010) Evolutionarily conserved regulatory mechanisms of abscisic acid signaling in land plants: characterization of ABSCISIC ACID INSENSITIVE1‐like type 2C protein phosphatase in the liverwort Marchantia polymorpha. Plant Physiology 152: 1529–1543.

Uddenberg D, Reimegård J, Clapham D, et al. (2013) Early cone setting in Picea abies acrocona is associated with increased transcriptional activity of aMADS box transcription factor. Plant Physiology 161: 813–823.

Uddenberg D, Akhter S, Ramachandran P, et al. (2015) Sequenced genomes and rapidly emerging technologies pave the way for conifer evolutionary developmental biology. Frontiers in Plant Science 6: 970.

Umen JG and Olson BJ (2012) Genomics of volvocine algae. Advances in Botanical Research 64: 185–243.

Vlad D, Kierzkowski D, Rast MI, et al. (2014) Leaf shape evolution through duplication, regulatory diversification, and loss of a homeobox gene. Science 343: 780–783.

Wichard T (2015) Exploring bacteria‐induced growth and morphogenesis in the green macroalga order Ulvales (Chlorophyta). Frontiers in Plant Science 6: 86.

Wichard T, Charrier B, Mineur F, et al. (2015) The green seaweed Ulva: a model system to study morphogenesis. Frontiers in Plant Science 6: 72.

Wickett NJ, Mirarab S, Nguyen N, et al. (2014) Phylotranscriptomic analysis of the origin and early diversification of land plants. Proceedings of the National Academy of Sciences of the United States of America 111: E4859–E4868.

Yasumura Y, Crumpton‐Taylor M, Fuentes S, et al. (2007) Step‐by‐step acquisition of the gibberellin‐DELLA growth‐regulatory mechanism during land‐plant evolution. Current Biology 17: 1225–1230.

Yasumura Y, Pierik R, Fricker MD, et al. (2012) Studies of Physcomitrella patens reveal that ethylene‐mediated submergence responses arose relatively early in land‐plant evolution. Plant Journal 72: 947–959.

Yasumura Y, Pierik R, Kelly S, et al. (2015) An ancestral role for constitutive triple response 1 proteins in both ethylene and abscisic acid signaling. Plant Physiology 169: 283–298.

Further Reading

Bowman JL (2015) A brief history of Marchantia: from Greece to genomics. Plant Cell Physiology. DOI: 10.1093/pcp/pcv044.

Bryan GJ and Hein I (2008) Genomic resources and tools for gene function analysis in potato. International Journal of Plant Genomics. DOI: 10.1155/2008/216513.

Harholt J, Moestrop Ø and Ulvskov P (2016) Why plants were terrestrial from the beginning. Trends in Plant Science 21: 96–101.

Hochholdinger F and Zimmerman R (2008) Conserved and diverse mechanisms in root development. Current Opinion in Plant Biology 11: 70–74.

Kirk DL (2005) A twelve‐step program for evolving multicellularity and a division of labor. Bioessays 27: 299–310.

Marcon C, Paschold A and Hochholdinger F (2013) Genetic control of root organogenesis in cereals. Methods in Molecular Biology 959: 69–981.

Mysore KS, Tuori RP and Martin GB (2001) Arabidopsis genome sequence as a tool for functional genomics in tomato. Genome Biology 2: reviews 1003.1–reviews 1003.4.

Paterson AH, Freeling M and Sasaki T (2005) Grains of knowledge: genomics of model cereals. Genome Research 15: 1643–1650.

Umen JG (2014) Green algae and the origins of multicellularity in the plant kingdom. Cold Spring Harbor Perspectives in Biology 6: a016170.

Wang Y and Li J (2008) Molecular basis of plant architecture. Annual Review of Plant Biology 59: 253–279.

Contact Editor close
Submit a note to the editor about this article by filling in the form below.

* Required Field

How to Cite close
Coates, Juliet C(Jun 2016) Model Plants for Understanding Evolution. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0023749]