Exploring the evolution of plants from water to land
In this excerpt from Evolutionary Biology: A Plant Perspective, Mitchell Cruzan explores the transition of plant life from aquatic to terrestrial environments.
Toward the end of the Neoproterozoic, producers were so abundant in aquatic environments that the low availability of resources limited population growth. In deep-water habitats there was insufficient light, and in shallower water there was a severe lack of inorganic nutrients (primarily nitrogen and phosphorous). While nutrients were more abundant out of the water, they remained inaccessible for most aquatic life.
Transition from aquatic to terrestrial environments required overcoming seemingly insurmountable obstacles: severe desiccation, large temperature fluctuations, intense solar radiation, and the effects of gravity, all of which rendered the terrestrial environment deadly for most aquatic life forms.
At the same time, there was strong selection to overcome these impediments as the ability to tolerate exposure to dry air afforded access to ample light and more abundant nutrients. The first algal lineages that ultimately persisted and thrived out of water sparked the diversification of numerous terrestrial groups.
The emergence of green life from the water was inevitable — the more abundant resources available on land were not likely to remain unexploited for long. The ancestors of land plants — the charophyte algae — were probably dependent on precipitation and runoff from dry land as the primary source of inorganic nutrients. With nutrient availability as a primary limitation to plant growth in the water, it was just a matter of time before the appropriate innovations appeared to allow colonization of terrestrial habitats. Survival on land required overcoming severe drying and exposure to sunlight; strong selection gradients existed at the water’s edge where periodic exposure favored desiccation resistance. Under these circumstances any adaptations that improved tolerance to drying or the extraction of water and nutrients from the substrate would have spread, allowing early colonizers to incrementally invade drier habitats.
These first stages of transition to terrestrial habitats remain entirely unknown. There are no living plants that retain the morphological characteristics of the earliest land plants, and we do not have any fossils that can definitively be associated with transitional forms. While plants in the Bryophyta (mosses, liverworts, and hornworts) are often referred to as representatives of the earliest land plants, they actually are quite divergent and possess a number of complex traits that make them much more similar to other land plants than to streptophyte algae.
The characteristics shared among bryophyte groups include a multicellular sporophyte, parenchymous (i.e., undifferentiated cell) growth of the gametophyte, apical growth, and complex reproductive structures. The commonality of these traits among bryophyte lineages suggests that the common ancestor they share with other land plants (vascular plants, the Tracheophyta) probably possessed the same set of traits.
On the other hand, Bryophytes differ from other vascular plants by having a dominant gametophyte stage, a dependent sporophyte stage, and the lack of true vascular tissue (Tracheids). Sporophytes and gametophytes of some mosses possess conducting cells (Hydroids) that serve as vascular tissue, but since most bryophyte lineages do not have this feature, it is more likely that hydroids are independently derived and not homologous to the vascular tissue of the tracheophytes. This scenario is supported by the observation that conducting cells in moss sporophytes and liverwort gametophytes lack the cell wall thickenings and lignification present in the tracheids of vascular plants.
By considering the distribution of shared traits among extant lineages of embryophytes and streptophyte algae, we can make some logical guesses about the probable characteristics of the first land plants.
We can infer that the first fully terrestrial lineages were small plants that had a dominant gametophyte stage, and a diploid stage that was either a unicellular zygote or a simple multicellular sporophyte that was dependent on the gametophyte (traits shared with bryophytes and streptophyte algae). The gametophyte stage was probably a Thallus (a flat plant body consisting of undifferentiated cells, lacking specialized tissues and organs) that had apical growth and unicellular Rhizoids (hair- like extensions of cells that serve the same function as roots) — traits shared with the gametophytes of hornworts, liverworts, lycopods, and ferns.
These plants were restricted to areas of constant moisture, as they possessed little capacity to maintain their internal water status.
The picture that emerges for the first terrestrial plants is one of small, thalloid gametophytes with limited ability to maintain their internal water status and so remaining closely appressed to a moist substrate. These plants had a dominant gametophyte stage and probably produced motile sperm, so they required water for successful reproduction. The diploid stage would have been a unicellular zygote (similar to charophyte algae) or a reduced multicellular sporophyte (similar to liverworts). These first terrestrial plants may have been limited to locations with consistent moisture availability and some shade until adaptations appeared that allowed them to survive in more exposed sites.
As terrestrial lineages spread and became more abundant, competition would have ensued as habitat space with sufficient moisture became limiting to growth. Selection on terrestrial populations would have favored traits that contributed to their ability to colonize new habitat and to compete with other members of the plant community.
Mitchell B. Cruzan is Professor of Biology at Portland State University.
