How land plant life cycles first evolved

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Science  22 Dec 2017:
Vol. 358, Issue 6370, pp. 1538-1539
DOI: 10.1126/science.aan2923

This year marks the 100th anniversary of the first in a series of papers on the biota of a 407-million-year-old hot spring system that opened a window onto early life on land (1). The site near the village of Rhynie in Aberdeenshire, Scotland, is exceptional because fossilization occurred in microcrystalline silica (chert), preserving organisms to the cellular level and shedding light on community structure and interactions among the plants, arthropods, fungi, algae, and cyanobacteria. Recent research on these remarkable fossils and advances in understanding plant developmental genetics are beginning to reveal how major changes in life cycle had an early influence on the direction of plant evolution.

When the Rhynie Chert fossils were first reported, the plants, in particular, caused quite a stir because they seemed to capture an early stage in the adaptation to life on land. Most lack key organs familiar in living species, such as leaves or roots. Moreover, they are small (<20 cm), with simple bifurcating axes that terminate in spore-bearing sacs. Later research has revealed that their life cycles also differed in important ways from those of living species.

Land plants inherited their biochemistry and cell biology from ancestral green algae, but their fundamental organs and tissues evolved on land. Their closest algal relatives have a haplontic life cycle, which typically features a simple multicellular haploid sexual phase (a gametophyte) and a unicellular diploid zygote (2). This implies that the ancestor of land plants was also haplontic, probably with a filamentous, weakly differentiated multicellular phase (3).

The transition to land entailed changes in life cycle in which the diploid zygote also became multicellular (4). This change was accompanied by substantial somatic development, resulting in the evolution of tissues and organs basic to plants, such as stems, leaves, roots, a vascular system, stomata (the minute pores that facilitate gaseous exchange), and sex and dispersal organs. The multicellular diploid phase evolved into a highly successful spore-producing dispersal unit (the sporophyte), laying the foundations of modern plant diversity. Changes in life cycle thus underpinned the early diversification of plants on land, but how such changes evolved remains a puzzle.

Today, life cycles vary considerably among major plant lineages (4, 5). In bryophytes (mosses, liverworts, and hornworts), the sporophyte is a small stalked capsule that is nutritionally dependent on its parent, which is a cosexual or a female gametophyte of leafy or crustose type. In vascular plants (lycopods, ferns, gymnosperms, and flowering plants), the converse happens. The sporophytes are large, leafy, free-living plants. In flowering plants and gymnosperms, the female gametophyte is reduced to an ovule typically borne in a cone or a flower, and the male is reduced to motile sperm or a minute tube that grows from a pollen grain. By contrast, in ferns and lycopods, after a short period of embryonic development, the two parts of the life cycle become independent. The sporophyte is large and has well-developed leaves, roots, and vascular system, whereas the gametophyte is miniscule. It can be surficial and photosynthetic or subterranean and heterotrophic, but with very limited tissue development.

In phylogenetic terms, the bryophyte life cycle is thought to be intermediate between that of the algal ancestors and those of vascular plants (2, 4, 5). Scientists have therefore assumed that the life cycles of early plants would conform to the bryophyte or the fern and lycopod types, which are considered ancestral in vascular plants. But the Rhynie Chert fossils suggest otherwise.

Life-cycle phases are known in varying degrees of detail for four of the six fossil plant species from the Rhynie Chert. Like ferns, the gametophytes and sporophytes lived as independent plants, but unlike any living land plants, tissues such as rooting structures, a vascular system, and stomata were expressed in both parts of the life cycle (6). Despite these similarities, sporophytes and gametophytes were not identical. Although both were axial and leafless, the gametophytes were smaller. Overall, habit and size are still poorly understood for several gametophytes, but one factor known to influence their size was the degree of development of their branching systems (1). Also, in several species, gametophyte axes terminated in an expanded cup-shaped structure that bore the sexual organs. These differences notwithstanding, the gametophyte bore much greater similarity to the sporophyte than it does in living species, and it developed tissues of greater diversity.

Neither bryophytes nor ferns, these fossils elucidate a major early shift in life cycle that had far-reaching consequences for plant evolution. This shift involved the liberation of the sporophyte from complete physiological dependence on its gametophyte (a bryophyte life cycle) to achieve free-living status (a vascular plant life cycle). It entailed radical changes to the sporophyte's form and function. The fossils hint at how this transition might have taken place.

Molecular phylogenetic analysis of living species shows that the bryophytes are basal lineages in the land plant tree of life (2), implying that the basic features of the land plant body plan evolved initially in the gametophyte to create a multicellular free-living plant (see the figure) (5). Thus, the shift away from sporophyte nutritional dependency happened in the ancestors of all vascular plants. Phylogenetic analyses that include fossils consistently place the extinct Rhynie Chert species closer to the vascular plants than to the bryophytes. Like vascular plants, they all have free-living sporophytes with bifurcating axes. Some Rhynie Chert plants also possessed tracheids, which are distinctive water-conducting cells found only in vascular plants. These extinct life-cycle variants therefore most likely represent an ancestral condition of the vascular plants (6).

Unlike their living relatives, though, similar histology in the two parts of the fossil life cycles implies similar developmental processes and functions. This suggests that the mechanism behind the leap to sporophyte independence involved co-option by the sporophyte of those tissue systems that enabled the gametophyte to live as a fully independent autotroph (6). In this model, the sporophyte did not evolve novel structures to become free living and autotrophic; rather, the existing repertoire of gametophyte developmental with some limited redeployment in the reverse direction (for example, stomata).

How plant life cycles evolved

Plants that lived in the 407-million-year-old Rhynie Chert hot spring system had life cycles that were different from living species.


Evidence from developmental genetics lends support to this idea. A growing body of research points to the recruitment of ancient genes and gene regulatory networks early in land plant evolution from a preexisting gametophyte generation to the sporophyte (7). At the tissue and cellular levels, similar gene networks regulate root hair development in angiosperm sporophytes and the development of rhizoids (tip-growing rooting cells) in moss gametophytes (8). Likewise, the development of water-conducting cells is controlled by similar transcription factors in the angiosperm sporophyte and the moss gametophyte (9). Polar auxin transport, a key regulator of sporophyte ontogeny, is essential to organ and tissue patterning in the moss gametophyte (10, 11). These observations are consistent with ancient roles for these developmental regulators in the gametophyte. This fits with the Rhynie Chert life cycles, in which rhizoids and the vascular system are expressed in both life-cycle phases.

Not all findings of developmental genetics sit comfortably with the early fossil life cycles, however. In the life cycles of living plants, one genome gives rise to two distinct ontogenies. The gametophyte developmental program must be completely repressed in the sporophyte and vice versa. In moss, this is regulated by the expression of KNOX2 (KNOTTED-like TALE homeobox gene class II) in the sporophyte and PRC2 (polycomb repressive complex 2) complex genes in the gametophyte (12). In the Rhynie Chert life cycles, repression of sporophyte ontogeny in the gametophyte and vice versa is less complete. This implies differences in the downstream regulation of gene networks by KNOX2 and PRC2 complex genes in the fossils.

If shifting patterns of gene expression played an important role in transforming plant life cycles, they might also have brought together tissue systems and cell types that had initially evolved separately. Stomata are thought to have originated in the nutritionally dependent sporophytes of plants with bryophyte-like life cycles, in which their main role was to facilitate spore dispersal; they only later acquired a role in gaseous exchange in the vascular plants (13). By contrast, the vascular system and rhizoids probably evolved separately in the gametophyte (5). The shift in life cycle leading to the vascular plants brought rhizoids, vascular tissues, and stomata together in one developmental system for the first time. Thus, the key components that regulate transpiration were put in place in the vascular plants, forming a physiological platform of primary importance to their subsequent diversification.

The sporophyte of vascular plants came to dominate land floras, whereas the gametophyte has experienced progressive loss of tissues, beginning with the vascular system and stomata. One explanation of this divergence in form between the two phases of the life cycle is that the gametophyte evolved through a persistent, subterranean, mycotrophic phase, as seen in some basal groups of vascular plants today (14).

Direct fossil evidence for life cycles in early land plants is still very sparse. The developing understanding of the Rhynie Chert fossils provides a model for recognizing life cycles in less well-preserved but more abundant compression fossil floras. Direct evidence of life cycles in the earliest land plants before the Rhynie Chert fossils is limited to spores dispersed in sediments. These provide tantalizing glimpses. Unlike modern species in which most spores are dispersed as single grains, these earliest types were typically dispersed in packets of two or four, demonstrating that the packaging of the products of meiosis was more diverse than in plants today (15). Broader interrogation of the fossil record for further evidence of life-cycle diversity may yield more surprises.

References and Notes

Acknowledgments: I am indebted to D. Edwards, L. Dolan, and The Royal Society of London for funding an interdisciplinary discussion meeting on “Rhynie Chert—Our earliest terrestrial ecosystem revisited,” held in March 2017.
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