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Plant evolution and development in a post-genomic context

Key Points

  • Animal genome projects have sampled the animal kingdom from simple to complex organisms, whereas plant genome projects have concentrated on angiosperms. More comparative genomic information is needed before basic questions of plant evolution can be answered.

  • Plants have several unique features not found in animals, such as alternation of generations, no separation between soma and germ line, and endosperm formation controlled by imprinted and imprinting genes.

  • Several key transitions have occurred in plant evolution. The colonization of the land — the most important transition — was associated with several morphological innovations such as the stomata and the cuticle, increased morphological complexity and a KNOX (knotted-like homeobox) gene duplication.

  • The leaf has evolved many times. In seed plants, this has involved a collective of five genetic network innovations, in which KNOX genes, ASYMMETRIC LEAVES1 (a MYB transcription factor), PHANTASTICAB and REVOLUTA (both homeodomain-zip genes) are all implicated.

  • A characteristic plant class of MADS-box gene, the so-called MADS-IKC gene family, has diversified and this diversity has been recruited to specify identity in floral organs (the ABC model and its variants).

  • Bilateral (as opposed to radial) symmetry in flowers is a key innovation that promotes pollinator specialization. The gene CYCLOIDEA, which is asymmetrically expressed (on the adaxial side of the flower), is a key component of this phenomenon.

  • Selection on natural variation in cis-regulatory regions of transcriptional regulators might constitute an important driver of plant evolution. This mechanism has certainly been important in the evolution of cultivated maize from its domesticated ancestors.

  • Evolution of natural variation in flowering time in Arabidopsis shows how a single mutation (at the FRIGIDA locus) can have a profound effect on the ecology of a plant, shifting it from one adaptive peak to another.

  • Gene duplications are prevalent in plants and might lead to evolutionary innovation. The recent CYCLOIDEA/DICHOTOMA duplication in Antirrhinum contributes to the patterning of the specialized top petals of Antirrhinum. Some duplicate genes are apparently redundant, such as the SHATTERPROOF genes of Arabidopsis, but it is likely that very subtle divergence of function will be found between them.

  • New genomic tools will aid understanding of the evolution of gene networks. This will allow us to integrate the environment, the genotype and the phenotype into a post-genomic synthesis of plant evolution.

Abstract

Large-scale gene-sequencing projects that have been undertaken in animals have involved organisms from contrasting taxonomic groups, such as worm, fly and mammal. By contrast, similar botanical projects have focused exclusively on flowering plants. This has made it difficult to carry out fundamental research on how plants have evolved from simple to complex forms — a task that has been very successful in animals. However, in the flowering plants, the many completely or partially sequenced genomes now becoming available will provide a powerful tool to investigate the details of evolution in one group of related organisms.

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Figure 1: Summary of green-plant phylogeny.
Figure 2: Five-step hypothesis of seed-plant leaf evolution.
Figure 3: Function of CYCLOIDEA and DICHOTOMA in Antirrhinum (snapdragon) flower morphology.
Figure 4: Duplication of KNOX genes.

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Acknowledgements

I thank R. Bateman and two anonymous referees for constructive comments on the manuscript.

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PHAN

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FURTHER INFORMATION

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Glossary

BRYOPHYTE

Land plants in which the gametophyte generation is the larger, persistent phase. Bryophytes include the Hepaticophyta (liverworts), Anthocerotophyta (hornworts) and Bryophyta (mosses).

GAMETOPHYTE

The plant generation that has a haploid set of chromosomes and produces gametes.

SPOROPHYTE

The multicellular diploid form (in plants that undergo alternation of generations). The sporophyte results from a union of haploid gametes and meiotically produces haploid spores that grow into the gametophyte generation.

APOPLASTIC

Pertaining to the free space of tissue; specifically the cell wall porosity and intercellular spaces.

THALLUS

A cellular expansion that forms the main body of thalloid plants, such as algae and liverworts. Thalloid plants have no roots, stems or leaves, and include liverworts, hornworts and pteridophyte gametophytes.

STOMATA

Openings in the epidermis of a plant that permit gaseous exchange with the air. In general, all land plants except liverworts have stomata in their sporophyte stage.

MONOPODIAL

Growing continuously from a single growing point (meristem).

MERISTEM

A collection of stem cells in plants — undifferentiated but determined tissue, the cells of which are capable of active cell division and subsequent differentiation into specialized and permanent tissue, such as shoots and roots.

HETEROSPORY

The condition of producing two types of spore of different sizes: megaspores (female) and microspores (male).

LIGULE

An appendage on the upper side of a grass leaf at the point where the sheath joins the blade.

SPOROPHYLL

A leaf-like organ bearing sporangia (containing spores). The sporophyll and sporangia together form the basic reproductive unit of the sporophyte generation of land plants. Ovules of seed plants are derived from sporophylls and other organs, whereas the filament of the angiosperm stamens is a sporophyll.

CARPEL

The female reproductive organ of a flower.

STAMEN

The male organ of the angiosperm flower.

SPHENOPSIDS

A group of pteridophytes called horsetails, now represented by the extant genus Equisetum, but formerly much more diverse with many extinct woody forms. Pteridophytes comprise vascular plants in which both the gametophyte and sporophyte are free living. Other members of the group include the extant lycophytes and ferns, and many extinct groups, such as trimerophytes.

INDETERMINATE GROWTH

Continuation of the developmental history of an organism or organ when it reaches its adult form. This is characteristic of higher plants. By contrast, determinate growth describes the cessation of the developmental history of an organism or organ when it reaches its adult form. This is characteristic of higher animals.

PHENOLOGY

The timing of periodic biological phenomena that are usually correlated with climatic conditions.

NUCELLUS AND INTEGUMENT

The nucellus is the tissue that usually makes up the greater part of the ovule of seed plants. It encloses the embryo sac. It is itself enclosed by one or two protective coats called integuments, which become the seed coat.

SPORANGIUM

A reproductive structure in plants that produces spores by meoisis; in angiosperms, the anthers are groups of four sporangia.

EUDICOTS

The largest clade of angiosperms, characterized by three symmetrically placed pollen apertures or aperture arrangements derived from this.

SEPAL

Sepals form the outer ring of modified leaves that surrounds the petals, stamens and carpels.

PERIANTH

A collective term for all the external parts of the flower: the calyx, or sepals, and the corolla, or petals.

LODICULE

Plug or flap of tissue in the grass flower that occurs between the stamens and the bracts that enclose the flower, swelling rapidly to open the flower.

PAPPUS

A group of modified sepals often in the form of a ring of silky or bristly hairs, or scales.

XEROPHYTE

A plant adapted for growth under arid conditions.

HALOPHYTE

A salt-tolerant terrestrial plant.

APICAL DOMINANCE

The tendency for the apical meristem of a plant to be more active than its lateral or axial meristems. It is particularly evident in young trees and is due to the production of auxins (plant hormones) in the apical meristem.

SELECTIVE SWEEP

Process by which new favourable mutations become fixed so quickly that physically linked alleles also become fixed by 'hitchhiking'.

EPIMUTATION

A heritable change in gene expression but not gene sequence. This usually takes place by abnormally increasing the methylation status of a gene, producing a loss-of-function phenotype. This can then be heritable for many generations, unless reset by meiosis.

FITNESS PEAK

A phenotype or part of the possible morphological variation that has high fitness.

ADAPTIVE LANDSCAPE

If all morphological variation or all possible phenotypes are considered as a landscape some will have high fitness (peaks) and others low fitness (valleys).

COROLLA

Whorl of floral leaves (petals) that surround the stamens. They are usually coloured and attract pollinators, and may be joined into a tube or ring, as in advanced eudicots.

REPLUM

Septum dividing the ovary of crucifers (such as Arabidopsis) into chambers.

VALVE

Part of the ovary wall, at which splitting occurs to release the seeds.

MUTATIONAL LOAD

Negative fitness consequence of naturally occurring mutations.

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Cronk, Q. Plant evolution and development in a post-genomic context. Nat Rev Genet 2, 607–619 (2001). https://doi.org/10.1038/35084556

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