The Evolution of Land Plants: Their Origin (in freshwater) and Radiation (on dry soil)

I. Origin of Land Plants: when green algae crawled out of water.

Evolutionary Timescale of Life on Earth

Scientists estimate that microscopic life emerged on planet Earth more than 4 billion years ago, right after the formation of the oceans. Embryophytes (Bryophytes or non-vascular plants and Tracheophytes or vascular plants), commonly known as land plants, originated 600 million years ago (MYA) from a photosynthetic organism likely related to extant Charophyte green algae (Figure 1).

Figure 1. Sketching the evolutionary history of land plants. Schematic representation of the green lineage evolution from chlorophytes to streptophytes. Embryophytes presumably derived from a filamentous algal ancestor that gradually adapted to dry soils. Image by Debbie Maizels (Zoobotanica Scientific Illustration: www.scientific-art.com), adapted from Figure 1 (de Vries and Archibald, 2018).

Invasion of Land Plants: key physiological features and life history traits

The algal ancestors of land plants progressively evolved complex characteristics that favoured the transition from aquatic to terrestrial habitats (i.e., terrestrialization). The gradual adaptation to dry soil relied on novel physiological traits that allowed organisms to cope with environmental stresses, such as tolerance to desiccation and fluctuating temperatures or protection against UV light and high irradiance.

The success of land colonization by early plants also leaned on the alternation of two generations: the haploid gametophyte (bearing gametes) with one set of genetic information and the diploid sporophyte (bearing spores) with two sets of genetic information. Intriguingly, land plants developed specialized parental tissues to protect and nourish the sporophyte within the gametophyte upon fertilization.

Impact of Plants on Planet Earth

Land plant colonization has transformed the geology of the planet. As photosynthetic organisms, plants have changed the carbon cycle and altered the composition of the atmosphere by reducing CO2 and increasing O2. These biogeochemical and atmospheric changes also made the evolution of animal life on the Earth’s surface possible.

How to Study Plant Evolution

PALAEOBOTANY studies fossil records of primitive plants. Based on the analysis of crypto spores, the divergence between bryophytes and tracheophytes was traced back to 462 million years ago (MYA). However, critical time points could be underestimated: in a species, genetic changes occurred long before the appearance of phenotypic novelties that mark the diversification of the lineages!

Complementary to this approach, COMPARATIVE GENOMICS identifies similarities and differences among lineages by studying the DNA of different species. Sequencing the genomes of extant green organisms related to the plant ancestors revealed a more ancient origin of the “genetic toolkit” associated with key innovations that allowed land invasion.

A molecular clock is a tool used to “calculate” the divergence date between two lineages. If DNA sequences change at a constant rate over the years, the genetic differences between two species should be proportional to the time they shared a common ancestor. To estimate evolutionary timescales, the clock should be “calibrated” using fossil records or known geological events.

II. Radiation of Land Plants: from small algal scum to big forests & flower gardens

Evolutionary Innovations in Streptophytes

During the evolutionary history of Viridiplantae (green plants), the two major lineages Chlorophyta – green algae that mainly lived in marine environments – and Streptophyta – green algae that preferred freshwater and land plants that colonized terrestrial environments – diverged more than 800 MYA (Figure 2). These latter organisms were able to expand their habitats as they developed composite cell walls, which contributed to the structural and functional integrity of cells in different conditions.

**Figure 2.** Early evolution of *Viridiplantae*. Left, the divergence between Chlorophyta (living in marine habitats) and Streptophyta (living in freshwater) in the Neoproterozoic era (more than 500 MYA). Right, Phylogenetic analysis of the relationships among Chlorophytes and Streptophytes. Embryophytes are related to Charales, Coleochaetales and Zygnematales. Images adapted from Figures 1 and 2 (Becker and Marin, 2009).

The ancestors of land plants were photoautotrophic organisms that first acquired increasing complexity through multicellularity. Over million years, plant evolution also encompassed the appearance of novel physiological, morphological, and developmental features. Besides the gradual shift from humid environments close to freshwater to dry environments with seasonal rainfall, land plant ancestors also modified their life cycle through alternating haploid/diploid generations; supporting this hypothesis, extant Charophyte green algae alternate a multicellular haploid generation (gametophyte) with a unicellular diploid generation (sporophyte) – produced by the fusion of two spores and protected by a cell layer. Ultimately, evolutionary changes also include the transition from the dispersal of spores to the dispersal of seeds that better tolerate a wide range of environmental limitations, thus promoting the perpetuation of the species even in harsh conditions.

From Embryophytes to Spermatophytes

Based on the analysis of fossil records, it is estimated that EMBRYOPHYTES (plants producing embryos) dominated the planet 470 MYA. The hallmark of these early land plants is the appearance of the heteromorphic life history trait: male and female gametophytes (1n) produce haploid sperm cells (in antheridium) and egg cells (in archegonium), respectively, which fuse to form a diploid sporophyte (2n). Haploid gametophytes live on the ground to facilitate oogamous sexual reproduction: fertilization occurs in the presence of water when small motile (male) gametes swim and fuse with bigger non-motile (female) gametes. Upon fertilization, the zygotes are retained within the parental tissue, which protects and nourishes the developing embryos. The sporophyte (2n) undergoes meiosis to produce haploid spores (1n), which later develop new gametophytes by mitosis.

The terminal sporangium (a capsule that stores the spores) promotes the long-range dispersal of spores, which are covered by a material called sporopollenin that confers protection from external agents (e.g., UV light, chemical or physical threads). Therefore, embryo formation represents a key adaptation of the ancestral precursor of plants to terrestrial ecosystems. Embryophytes also evolved apical growth, optimized the control of gas exchange and water loss through small apertures (stomata), and increased tolerance to desiccation through a waterproof outer layer (cuticle).

Bryophytes (liverworts, mosses, hornworts) are a living example of early embryophytes (Figure 3) showing key evolutionary innovations: the transition from 2D to 3D growth, the development of leaf-like structures and rhizoid filaments (as anchorage system), and dominance of haploid gametophyte in the life cycle.

**Figure 3. Examples of extant bryophytes.** The moss *Physcomitrium patens* (left) is used as model species in comparative studies to investigate plant evolution as it shares essential processes underlying plant development and physiology. Other examples are the liverwort *Marchantia polymorpha* (middle) which lives in damp habitats and shows separate male/female individuals, and the hornwort *Anthoceros agrestis* (right), which lives in moist soil and produces a horn-like cylindrical structure bearing spores.
*Physcomitrium patens*. Image: Pirex / Wikimedia Commons.
*Marchantia polymorpha*. Image: Krzysztof Ziarnek, Kenraiz / Wikimedia Commons.
*Anthoceros agrestis*. Image: HermannSchachner / Wikimedia Commons.

TRACHEOPHYTES (plants producing vascular tissues) appeared 440-415 MYA. The vasculature represents an efficient system to transport water/nutrients from the soil to the plant body and photosynthates from the leaf to other plant organs. The vascular plants’ lineage also evolved specialized leaves and roots, which serve not only to anchor the plant to the ground but also to penetrate the soil for nutrient uptake. Transformations in body plans were accompanied by a shift in the life cycle from gametophytic-dominant in non-vascular plants to sporophytic-dominant in vascular plants.

Pteridophytes (ferns and lycophytes) are simple vascular plants (Figure 4) showing differentiation of vascular tissues (xylem, phloem), the dominance of the sporophyte (usually asexual and diploid) in the life cycle, but still reproduction by spore dispersion.

**Figure 4. Examples of extant Pteridophytes.** Lycophytes suffered a massive extinction 300 MYA, and only 1,200 species of the orders *Lycopodiales* (left), *Selaginellales* (middle), *Isoetales* (right) still survive to date.
*Lycopodium annotinum*. Image: Jerzy Opioła / Wikimedia Commons.
*Selaginella moellendorffii*. Image: Gribskov / Wikimedia Commons.
Isoetes melanospora. Image: AHR12 / Wikimedia Commons.

SPERMATOPHYTES (plants producing seeds) emerged 370-300 MYA and differentiated separate female-like megaspores and male-like microspores. In the seed plants lineage, sexual reproduction occurs by fertilization: a sperm cell fuses with an egg cell to give rise to an embryo, which is protected and nourished by inner and outer layers of parental origin. The embryo and surrounding layers constitute the SEED. Seed plants are classified as Gymnosperms if they produce “naked seeds” or Angiosperms if they produce seeds protected by a fruit.

Gymnosperms (cycads, conifers, gnetophytes, ginkgo) appeared early in evolution (~390 MYA) and produce two types of cones (pollen, ovulate) bearing unisexual reproductive structures. Except for cycads, gymnosperms produce wood from the cambium.

Angiosperms appeared later in evolution (145-100 MYA) and form hermaphrodite flowers containing both male and female reproductive organs. In the flowering plants’ lineage, sexual reproduction occurs by double fertilization. In addition to the formation of the embryo, a second haploid sperm cell fuses with a diploid central cell to give rise to a triploid endosperm that nourishes the embryo. At maturity, developing seeds are enclosed within a fruit.

*Cycas revoluta*, male. Image: Danorton / Wikimedia Commons.
*Cycas revoluta*, female. Image: Rickjpelleg / Wikimedia Commons.
*Petunia exserta*. Image: Scott Zona / Wikimedia Commons.

Figure 5. Examples of Gymnosperms and Angiosperms

SUGGESTED READING

Becker, B. and Marin, B. (2009) “Streptophyte algae and the origin of embryophytes,” Annals of Botany, 103(7), pp. 999–1004. Available at: https://doi.org/10.1093/aob/mcp044.

Bowles, A.M.C., Williamson, C.J., Williams, T.A., Lenton, T.M. and Donoghue, P.C.J. (2023) “The origin and early evolution of plants,”Trends in Plant Science, 28(3), pp. 312–329. Available at: https://doi.org/10.1016/j.tplants.2022.09.009.

Bowman, J.L. (2022) “The origin of a land flora,” Nature Plants, 8(12), pp. 1352–1369. Available at: https://doi.org/10.1038/s41477-022-01283-y.

Domozych, D.S., Popper, Z.A. and Sørensen, I. (2016) “Charophytes: Evolutionary giants and emerging model organisms,” Frontiers in Plant Science, 7, p. 1470. Available at: https://doi.org/10.3389/fpls.2016.01470.

Donoghue, P.C.J., Harrison, C.J., Paps, J. and Schneider, H. (2021) “The evolutionary emergence of land plants,” Current Biology, 31(19), pp. R1281–R1298. Available at: https://doi.org/10.1016/j.cub.2021.07.038.

de Vries, J. and Archibald, J.M. (2018) “Plant evolution: landmarks on the path to terrestrial life,” New Phytologist, 217(4), pp. 1428–1434. Available at: https://doi.org/10.1111/nph.14975.