Abstract:SignificanceEstablishing the timescale of early land plant evolution is essential to testing hypotheses on the coevolution of land plants and Earth’s System. Here, we establish a timescale for early land plant evolution that integrates over competing hypotheses on bryophyte−tracheophyte relationships. We estimate land plants to have emerged in a middle Cambrian–Early Ordovocian interval, and vascular plants to have emerged in the Late Ordovician−Silurian. This timescale implies an early establishment of terres… Show more
“…Size of major land plant clades is according to species numbers reported in Christenhusz and Byng (). Phylogenetic relationships and divergence times follow Puttick et al () and Morris et al (). (b) Evolution of trophic modes and mycorrhizal associations in Burmannia (Burmanniaceae).…”
Section: Multiple Origins Of Full Mycoheterotrophymentioning
Since the early colonization of land, plants depend, to various extents, on mycorrhizal fungi to meet their nutrient demands. In most mycorrhizal symbioses, plants provide sugars derived from photosynthesis to the fungi, whereas the fungi provide essential minerals to the plant. However, in some plants, the flow of carbon has reversed and the fungi provide carbon to the plants. These plants are called mycoheterotrophs. However, it remains unclear how and under which circumstances trophic modes change and whether transitions in trophic modes are associated with changes in mycorrhizal communities.
Here, we review the available literature on mycorrhizal associations and trophic modes in plants. We first outline how trophic modes can be determined and how they differ across plants. We then investigate the evolutionary context under which mycoheterotrophy originated. We also examine the mycorrhizal communities associating with autotrophic, partially mycoheterotrophic and fully mycoheterotrophic plants within different plant families and investigate whether commonalities can be observed.
Our overview shows that mycoheterotrophy has originated more than 40 times through evolutionary time and can be found in a wide range of plant groups, including liverworts, lycophytes, ferns, monocots and dicots. Partial mycoheterotrophy appears to be much more common than previously anticipated and represents an almost continuous gradient between autotrophy and full mycoheterotrophy.
Comparison of the mycorrhizal communities associating with autotrophic, partial and full mycoheterotrophic plants indicates that, although they share some commonalities, shifts from autotrophy to full mycoheterotrophy are accompanied by either losses or shifts in mycorrhizal partners, suggesting that full or partial loss of photosynthesis selects for different mycorrhizal communities.
Synthesis. Partial mycoheterotrophy appears to be much more common than previously thought and represents an almost continuous gradient from autotrophy to full mycoheterotrophy. Evolution to full mycoheterotrophy is challenging as it requires specific adaptations and often a switch to other mycorrhizal partners. More detailed analyses of the functionality of different mycorrhizal systems co‐occurring in the roots of a single plant and the costs of mycorrhizal switching are needed to understand the precise mechanisms leading to full mycoheterotrophy.
“…Size of major land plant clades is according to species numbers reported in Christenhusz and Byng (). Phylogenetic relationships and divergence times follow Puttick et al () and Morris et al (). (b) Evolution of trophic modes and mycorrhizal associations in Burmannia (Burmanniaceae).…”
Section: Multiple Origins Of Full Mycoheterotrophymentioning
Since the early colonization of land, plants depend, to various extents, on mycorrhizal fungi to meet their nutrient demands. In most mycorrhizal symbioses, plants provide sugars derived from photosynthesis to the fungi, whereas the fungi provide essential minerals to the plant. However, in some plants, the flow of carbon has reversed and the fungi provide carbon to the plants. These plants are called mycoheterotrophs. However, it remains unclear how and under which circumstances trophic modes change and whether transitions in trophic modes are associated with changes in mycorrhizal communities.
Here, we review the available literature on mycorrhizal associations and trophic modes in plants. We first outline how trophic modes can be determined and how they differ across plants. We then investigate the evolutionary context under which mycoheterotrophy originated. We also examine the mycorrhizal communities associating with autotrophic, partially mycoheterotrophic and fully mycoheterotrophic plants within different plant families and investigate whether commonalities can be observed.
Our overview shows that mycoheterotrophy has originated more than 40 times through evolutionary time and can be found in a wide range of plant groups, including liverworts, lycophytes, ferns, monocots and dicots. Partial mycoheterotrophy appears to be much more common than previously anticipated and represents an almost continuous gradient between autotrophy and full mycoheterotrophy.
Comparison of the mycorrhizal communities associating with autotrophic, partial and full mycoheterotrophic plants indicates that, although they share some commonalities, shifts from autotrophy to full mycoheterotrophy are accompanied by either losses or shifts in mycorrhizal partners, suggesting that full or partial loss of photosynthesis selects for different mycorrhizal communities.
Synthesis. Partial mycoheterotrophy appears to be much more common than previously thought and represents an almost continuous gradient from autotrophy to full mycoheterotrophy. Evolution to full mycoheterotrophy is challenging as it requires specific adaptations and often a switch to other mycorrhizal partners. More detailed analyses of the functionality of different mycorrhizal systems co‐occurring in the roots of a single plant and the costs of mycorrhizal switching are needed to understand the precise mechanisms leading to full mycoheterotrophy.
“…Hence, during terrestrialization >500 million years ago [see [45] for the latest dating] one can imagine that the earliest land plants would have encountered a very different set of microbes than those in the freshwater environments from which they were emerging. Yet, a fluent passage scenario seems equally reasonable if one considers, e.g., a freshwater environment (microbe load A) that routinely dried out (microbe load B).…”
Section: Ancient Land Plant-microbe Interactions and Evidence From Momentioning
confidence: 99%
“…Since most data have been gathered for angiosperms, we will use them primarily for comparative purposes.10.1080/19420889.2018.1486168-F0001Figure 1.Key phytopathogen interaction factors across the trajectory of streptophyte evolution. Schematic cladogram (white lines) of the Chloroplastida depicts the deep split of the green lineage into Chlorophyta and Streptophyta about 900 million years ago (divergence times based on Morris et al [45]). The Streptophyta encompass the paraphyletic streptophyte algae and the monophyletic land plants (Embryophyta).…”
Section: Introductionmentioning
confidence: 99%
“…Schematic cladogram (white lines) of the Chloroplastida depicts the deep split of the green lineage into Chlorophyta and Streptophyta about 900 million years ago (divergence times based on Morris et al [45]). The Streptophyta encompass the paraphyletic streptophyte algae and the monophyletic land plants (Embryophyta).…”
All land plants must cope with phytopathogens. Algae face pathogens, too, and it is reasonable to assume that some of the strategies for dealing with pathogens evolved prior to the origin of embryophytes – plant terrestrialization simply changed the nature of the plant-pathogen interactions. Here we highlight that many potential components of the angiosperm defense toolkit are i) found in streptophyte algae and non-flowering embryophytes and ii) might be used in non-flowering plant defense as inferred from published experimental data. Nonetheless, the common signaling networks governing these defense responses appear to have become more intricate during embryophyte evolution. This includes the evolution of the antagonistic signaling pathways of jasmonic and salicylic acid, multiple independent expansions of resistance genes, and the evolution of resistance gene-regulating microRNAs. Future comparative studies will illuminate which modules of the streptophyte defense signaling network constitute the core and which constitute lineage- and/or environment-specific (peripheral) signaling circuits.
“…The idea that the origin of animals was ultimately controlled by changing environmental factors predicts a polyphyletic origin of animals [1,[31][32][33]. In this scenario, multiple eukaryotic lineages possessed the [44,56,63], Ascomycota [64], Basidiomycota [64], Embryophytes [65][66][67], and Laminarialeans [68]. References for and biomarkers earliest fossils: Metazoans [57,69,70], Florideophytes ([71] -though see [42]), Ascomycota [72], Basidiomycota [73], Embryophytes [74,75] and Laminarialeans [76].…”
Section: Introduction: the Neoproterozoic Origins Of Complex Multicelmentioning
The Neoproterozoic Era (1000-541 million years ago, Ma) was characterized by dramatic environmental and evolutionary change, including at least two episodes of extensive, low-latitude glaciation, potential changes in the redox structure of the global ocean, and the origin and diversification of animal life. How these different events related to one another remains an active area of research, particularly how these environmental changes influenced, and were influenced by, the earliest evolution of animals. Animal multicellularity is estimated to have evolved in the Tonian Period (1000-720 Ma) and represents one of at least six independent acquisitions of complex multicellularity, characterized by cellular differentiation, three-dimensional body plans, and active nutrient transport. Compared with the other instances of complex multicellularity, animals represent the only clade to have evolved from wall-less, phagotrophic flagellates, which likely placed unique cytological and trophic constraints on the evolution of animal multicellularity. Here, we compare recent molecular clock estimates with compilations of the chromium isotope, micropaleontological, and organic biomarker records, suggesting that, as of now, the origin of animals was not obviously correlated to any environmental-ecological change in the Tonian Period. This lack of correlation is consistent with the idea that the evolution of animal multicellularity was primarily dictated by internal, developmental constraints and occurred independently of the known environmental-ecological changes that characterized the Neoproterozoic Era.
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