Editing Mycorrhiza (section)

== Evolution ==

Fossil and genetic evidence indicate that mycorrhizae are ancient, potentially as old as the [[Timeline of plant evolution#Ordovician flora|terrestrialization of plants]]. Genetic evidence indicates that all land plants share a single common ancestor,<ref>{{Cite journal |last1=Harris |first1=Brogan J. |last2=Clark |first2=James W. |last3=Schrempf |first3=Dominik |last4=Szöllősi |first4=Gergely J. |last5=Donoghue |first5=Philip C. J. |last6=Hetherington |first6=Alistair M. |last7=Williams |first7=Tom A. |date=2022-09-29 |title=Divergent evolutionary trajectories of bryophytes and tracheophytes from a complex common ancestor of land plants |journal=Nature Ecology & Evolution |volume=6 |issue=11 |pages=1634–1643 |doi=10.1038/s41559-022-01885-x |pmc=9630106 |pmid=36175544|bibcode=2022NatEE...6.1634H }}</ref> which appears to have quickly adopted mycorrhizal symbiosis, and research suggests that proto-mycorrhizal fungi were a key factor enabling plant terrestrialization.<ref>{{Cite journal |last1=Puginier |first1=Camille |last2=Keller |first2=Jean |last3=Delaux |first3=Pierre-Marc |date=2022-08-29 |title=Plant–microbe interactions that have impacted plant terrestrializations |url=https://academic.oup.com/plphys/article/190/1/72/6596610 |journal=Plant Physiology |volume=190 |issue=1 |pages=72–84 |doi=10.1093/plphys/kiac258 |pmid=35642902 |pmc=9434271 }}</ref> The 400 million year old [[Rhynie chert]] contains an assemblage of fossil plants preserved in sufficient detail that arbuscular mycorrhizae have been observed in the stems of [[Aglaophyton|''Aglaophyton major'']], giving a lower bound for how late mycorrhizal symbiosis may have developed.<ref name="Remy et al." /> Ectomycorrhizae developed substantially later, during the [[Jurassic]] period, while most other modern mycorrhizal families, including orchid and ericoid mycorrhizae, date to the period of [[Flowering plant#Cretaceous|angiosperm radiation]] in the [[Cretaceous]] period.<ref>{{Cite journal |last1=Miyauchi |first1=Shingo |last2=Kiss |first2=Enikő |last3=Kuo |first3=Alan |last4=Drula |first4=Elodie |last5=Kohler |first5=Annegret |last6=Sánchez-García |first6=Marisol |last7=Morin |first7=Emmanuelle |last8=Andreopoulos |first8=Bill |last9=Barry |first9=Kerrie W. |last10=Bonito |first10=Gregory |last11=Buée |first11=Marc |last12=Carver |first12=Akiko |last13=Chen |first13=Cindy |last14=Cichocki |first14=Nicolas |last15=Clum |first15=Alicia |display-authors=3 |date=2020 |title=Large-scale genome sequencing of mycorrhizal fungi provides insights into the early evolution of symbiotic traits |journal=Nature Communications |volume=11 |issue=1 |pages=5125 |doi=10.1038/s41467-020-18795-w |pmc=7550596 |pmid=33046698 |bibcode=2020NatCo..11.5125M}}</ref> There is genetic evidence that the symbiosis between [[legume]]s and [[nitrogen-fixing bacteria]] is an extension of mycorrhizal symbiosis.<ref>{{Cite journal |last1=Provorov |first1=N. A. |last2=Shtark |first2=O. Yu |last3=Dolgikh |first3=E. A. |date=2016 |title=[Evolution of nitrogen-fixing symbioses based on the migration of bacteria from mycorrhizal fungi and soil into the plant tissues] |url=https://pubmed.ncbi.nlm.nih.gov/30024143 |journal=Zhurnal Obshchei Biologii |volume=77 |issue=5 |pages=329–345 |pmid=30024143}}</ref> The modern distribution of mycorrhizal fungi appears to reflect an increasing complexity and competition in root morphology associated with the dominance of angiosperms in the [[Cenozoic |Cenozoic Era]], characterized by complex ecological dynamics between species.<ref>{{Cite journal |last1=Brundrett |first1=Mark C. |last2=Tedersoo |first2=Leho |date=2018 |title=Evolutionary history of mycorrhizal symbioses and global host plant diversity |journal=New Phytologist  |volume=220 |issue=4 |pages=1108–1115 |doi=10.1111/nph.14976 |pmid=29355963 |doi-access=free }}</ref>

Mycorrhizal relationships were likely crucial in terrestrial plant colonization some 450-500 million years ago, suggesting that mycorrhizal relationships are coincident with the evolution of terrestrial flora.<ref>{{cite journal |last1=Cairney |first1=J.W.G. |title=Evolution of Mycorrhiza Systems |journal=Naturwissenschaften |date=December 2000 |volume=87 |issue=11 |page=467 |doi=10.1007/s001140050762 |pmid=11151665 |bibcode=2000NW.....87..467C }}</ref>  Mycorrhizal relationships have independently evolved from saprotrophic fungi a number of times, and in effect mycorrhizae have developed multiple modes of exchange between root cells and hyphae. There are three major forms of mycorrhizal relationships which have evolved independently of one another, the oldest being arbuscular mycorrhizae, followed by ectomycorrhizal relationships, and most recently ericoid mycorrhizal relationships. 

'''Arbuscular Mycorrhizae''' 

Arbuscular mycorrhizae are the oldest and most frequent form of mycorrhizal relationship.<ref>{{cite journal |last1=Cairney |first1=J.W.G. |title=Evolution of Mycorrhiza Systems |journal=Naturwissenschaften |date=December 2000 |volume=87 |issue=11 |page=468 |doi=10.1007/s001140050762 |pmid=11151665 |bibcode=2000NW.....87..467C }}</ref> Arbuscular mycorrhizae establish nutrient exchange through penetrating the root cortical cells of the host plant, making the relationship endomycorrhizal (inside the cell) as opposed to the later developed ectomycorrhizae (external nutrient exchange). Arbuscular mycorrhizae leave behind arbuscules, tree-like structures formed through hyphal penetration into the cell. Arbuscular mycorrhizae take on most angiosperms, some gymnosperms, pteridophytes, and nonvascular plants as plant hosts.<ref>{{cite journal |last1=Cairney |first1=J.W.G. |title=Evolution of Mycorrhiza Systems |journal=Naturwissenschaften |date=December 2000 |volume=87 |issue=11 |page=475 |doi=10.1007/s001140050762 |bibcode=2000NW.....87..467C }}</ref> 

Arbuscular mycorrhizas likely evolved alongside terrestrial plants approximately 450-500 million years ago when plants first began to colonize land.<ref>{{cite journal |last1=Cairney |first1=J.W.G. |title=Evolution of Mycorrhiza Systems |journal=Naturwissenschaften |date=December 2000 |volume=87 |issue=11 |page=468 |doi=10.1007/s001140050762 |pmid=11151665 |bibcode=2000NW.....87..467C }}</ref>  Some scholars suggest arbuscular mycorrhizal relationships originated between fungus-like protists and algae during this time.<ref>{{cite journal |last1=Cairney |first1=J.W.G. |title=Evolution of Mycorrhiza Systems |journal=Naturwissenschaften |date=December 2000 |volume=87 |issue=11 |page=467 |doi=10.1007/s001140050762 |pmid=11151665 |bibcode=2000NW.....87..467C }}</ref> Paramycorrhizae, mycorrhiza-like structures, have been observed in the Rhynie Chert, a 407 million-year-old piece of fossilized earth found in Scotland,<ref>{{cite journal |last1=Strullu-Derrien |first1=Christine |last2=Selosse |first2=Marc-André |last3=Kendrick |first3=Paul |last4=Martin |first4=Francis M. |title=The Origin and Evolution of Mycorrhizal Symbioses: from Paleomycology to Phylogenomics |journal=New Phytologist |date=14 January 2018 |volume=220 |issue=4 |page=1018 |doi=10.1111/nph.15076 |bibcode=2018NewPh.220.1012S |url=https://nph.onlinelibrary.wiley.com/doi/epdf/10.1111/nph.15076}}</ref> setting a lower bound for mycorrhizal relationships. The earliest root-confined arbuscular mycorrhizae observed come from a fossil where hyphae are seen colonizing the rootlet of an arborescent clubmoss, forming arbuscules.<ref>{{cite journal |last1=Strullu-Derrien |first1=Christine |last2=Selosse |first2=Marc-André |last3=Kendrick |first3=Paul |last4=Martin |first4=Francis M. |title=The Origin and Evolution of Mycorrhizal Symbioses: from Paleomycology to Phylogenomics |journal=New Phytologist |date=14 January 2018 |volume=220 |issue=4 |page=1017 |doi=10.1111/nph.15076 |pmid=29573278 |bibcode=2018NewPh.220.1012S |url=https://nph.onlinelibrary.wiley.com/doi/epdf/10.1111/nph.15076}}</ref> 

There is a strong consensus among paleomycologists that mycorrhizal fungi served as a primitive root system for early terrestrial plants. This is because, prior to plant colonization of land, soils were nutrient sparse and plants had yet to develop root systems.<ref>{{cite journal |last1=Cairney |first1=J.W.G. |title=Evolution of Mycorrhiza Systems |journal=Naturwissenschaften |date=December 2000 |volume=87 |issue=11 |page=467 |doi=10.1007/s001140050762 |pmid=11151665 |bibcode=2000NW.....87..467C }}</ref>  Without complex root systems, early terrestrial plants would have been incapable of absorbing recalcitrant ions from mineral substrates, such as phosphate, a key nutrient for plant growth.<ref>{{cite journal |last1=Maherali |first1=Hafiz |last2=Oberle |first2=Brad |last3=Stevens |first3=Peter F. |last4=Cornwell |first4=William K. |last5=McGlinn |first5=Daniel J. |title=Mutualism Persistence and Abandoment during the Evolution of the Mycorrhizal Synbiosis |journal=The American Naturalist |date=November 2016 |volume=188 |issue=5 |page=E114 |doi=10.1086/688675 |pmid=27788343 |bibcode=2016ANat..188E.113M |url=https://www.journals.uchicago.edu/doi/10.1086/688675}}</ref> There are a number of indicators that all land plants evolved from arbuscular mycorrhizal symbiosis. One strong indicator is that arbuscular mycorrhizae have been observed in the seedling stage of otherwise ectomycorrhizal partners, suggesting that arbuscular mycorrhizae may be able to infect almost any land plant given proper circumstances.<ref>{{cite journal |last1=Cairney |first1=J.W.G. |title=Evolution of Mycorrhiza Systems |journal=Naturwissenschaften |date=December 2000 |volume=87 |issue=11 |page=470 |doi=10.1007/s001140050762 |pmid=11151665 |bibcode=2000NW.....87..467C }}</ref>  Arbuscular mycorrhizal symbiosis occurs between plants and fungi in the division glomeromycota, which has been observed in almost every seed plant taxonomic division, or around 67% of species.<ref>{{cite journal |last1=Maherali |first1=Hafiz |last2=Oberle |first2=Brad |last3=Stevens |first3=Peter F. |last4=Cornwell |first4=William K. |last5=McGlinn |first5=Daniel J. |title=Mutualism Persistence and Abandoment during the Evolution of the Mycorrhizal Synbiosis |journal=The American Naturalist |date=November 2016 |volume=188 |issue=5 |page=E114 |doi=10.1086/688675 |pmid=27788343 |bibcode=2016ANat..188E.113M |url=https://www.journals.uchicago.edu/doi/10.1086/688675}}</ref> As arbuscular mycorrhizae show minimal host plant specificity, and described mycorrhizae species are likely capable of forming relationships with most host plant taxa, this also suggests that terrestrial plants and arbuscular mycorrhizae evolved with one another. 

'''Ectomycorrhizae''' 

Ectomycorrhizae are mycorrhizal relationships formed without the hyphae of the fungi penetrating the root cells of the host plant, instead forming a sheath around the root of the symbiont for nutrient exchange. The earliest confirmed ectomycorrhizal fossil dates back to the eocene approximately 48 million years ago,<ref>{{cite journal |last1=Strullu-Derrien |first1=Christine |last2=Selosse |first2=Marc-André |last3=Kendrick |first3=Paul |last4=Martin |first4=Francis M. |title=The Origin and Evolution of Mycorrhizal Symbioses: from Paleomycology to Phylogenomics |journal=New Phytologist |date=14 January 2018 |volume=220 |issue=4 |page=1020 |doi=10.1111/nph.15076 |bibcode=2018NewPh.220.1012S |url=https://nph.onlinelibrary.wiley.com/doi/epdf/10.1111/nph.15076}}</ref> However it’s believed that the first ectomycorrhizal relationships evolved in the stem group Pinaceae around the radiation of the Pinaceae crown group in the mid Jurassic, 175 million or so years ago. <ref>{{cite journal |last1=Strullu-Derrien |first1=Christine |last2=Selosse |first2=Marc-André |last3=Kendrick |first3=Paul |last4=Martin |first4=Francis M. |title=The Origin and Evolution of Mycorrhizal Symbioses: from Paleomycology to Phylogenomics |journal=New Phytologist |date=14 January 2018 |volume=220 |issue=4 |page=1020 |doi=10.1111/nph.15076 |bibcode=2018NewPh.220.1012S |url=https://nph.onlinelibrary.wiley.com/doi/epdf/10.1111/nph.15076}}</ref>

Ectomycorrhizal relationships have evolved a number of times, in both plants and fungi. In angiosperms, it is believed that ectomycorrhizal partnerships have evolved independently at least 18 times, and in fungi 78-82 times.<ref>{{cite journal |last1=Strullu-Derrien |first1=Christine |last2=Selosse |first2=Marc-André |last3=Kendrick |first3=Paul |last4=Martin |first4=Francis M. |title=The Origin and Evolution of Mycorrhizal Symbioses: from Paleomycology to Phylogenomics |journal=New Phytologist |date=14 January 2018 |volume=220 |issue=4 |page=1020 |doi=10.1111/nph.15076 |bibcode=2018NewPh.220.1012S |url=https://nph.onlinelibrary.wiley.com/doi/epdf/10.1111/nph.15076}}</ref> The main evolutionary driver for ectomycorrhizae is switching of nutritional modes from saprotrophs.<ref>{{cite journal |last1=Strullu-Derrien |first1=Christine |last2=Selosse |first2=Marc-André |last3=Kendrick |first3=Paul |last4=Martin |first4=Francis M. |title=The Origin and Evolution of Mycorrhizal Symbioses: from Paleomycology to Phylogenomics |journal=New Phytologist |date=14 January 2018 |volume=220 |issue=4 |page=1022 |doi=10.1111/nph.15076 |pmid=29573278 |bibcode=2018NewPh.220.1012S |url=https://nph.onlinelibrary.wiley.com/doi/epdf/10.1111/nph.15076}}</ref> Phylogenomic analysis of various ectomycorrhizal fungal genomes has confirmed the 
convergent evolution of ectomycorrhizal fungi from white and brown-rot fungi, as well as from soil saprotrophs – Ectomycorrhizal fungi likely evolved convergently from saprotrophic origins several times.<ref>{{cite journal |last1=Strullu-Derrien |first1=Christine |last2=Selosse |first2=Marc-André |last3=Kendrick |first3=Paul |last4=Martin |first4=Francis M. |title=The Origin and Evolution of Mycorrhizal Symbioses: from Paleomycology to Phylogenomics |journal=New Phytologist |date=14 January 2018 |volume=220 |issue=4 |page=1022 |doi=10.1111/nph.15076 |pmid=29573278 |bibcode=2018NewPh.220.1012S |url=https://nph.onlinelibrary.wiley.com/doi/epdf/10.1111/nph.15076}}</ref><ref>{{cite journal |last1=Cairney |first1=J.W.G. |title=Evolution of Mycorrhiza Systems |journal=Naturwissenschaften |date=December 2000 |volume=87 |issue=11 |page=470 |doi=10.1007/s001140050762 |pmid=11151665 |bibcode=2000NW.....87..467C }}</ref>  Some lineages of ectomycorrhizae have likely evolved from endophytic ancestors, fungi that live within plants without damaging them, while others such as Amanitaceae evolved from saprotrophs.<ref>{{cite journal |last1=Strullu-Derrien |first1=Christine |last2=Selosse |first2=Marc-André |last3=Kendrick |first3=Paul |last4=Martin |first4=Francis M. |title=The Origin and Evolution of Mycorrhizal Symbioses: from Paleomycology to Phylogenomics |journal=New Phytologist |date=14 January 2018 |volume=220 |issue=4 |page=1022 |doi=10.1111/nph.15076 |pmid=29573278 |bibcode=2018NewPh.220.1012S |url=https://nph.onlinelibrary.wiley.com/doi/epdf/10.1111/nph.15076}}</ref> Some ectomycorrhizal fungi have gone through apparent evolutionary reversal back into saprotrophic ecology. This is possible because ectomycorrhizal fungi retain enzymes for breaking down lignin.<ref>{{cite journal |last1=Cairney |first1=J.W.G. |title=Evolution of Mycorrhiza Systems |journal=Naturwissenschaften |date=December 2000 |volume=87 |issue=11 |page=471 |doi=10.1007/s001140050762 |bibcode=2000NW.....87..467C }}</ref>  Most ectomycorrhizal relationships are formed between basidiomycetes or ascomycetes and woody trees or shrubs.<ref>{{cite journal |last1=Cairney |first1=J.W.G. |title=Evolution of Mycorrhiza Systems |journal=Naturwissenschaften |date=December 2000 |volume=87 |issue=11 |page=469 |doi=10.1007/s001140050762 |bibcode=2000NW.....87..467C }}</ref>    


'''Ericoid Mycorrhizae'''

Ericoid mycorrhizae evolved from a monophyletic origin around 140 million years ago.<ref>{{cite journal |last1=Cairney |first1=J.W.G. |title=Evolution of Mycorrhiza Systems |journal=Naturwissenschaften |date=December 2000 |volume=87 |issue=11 |page=471 |doi=10.1007/s001140050762 |bibcode=2000NW.....87..467C }}</ref>  The earliest ericoid mycorrhizae evolved from saprotrophic ascomycetes.<ref>{{cite journal |last1=Cairney |first1=J.W.G. |title=Evolution of Mycorrhiza Systems |journal=Naturwissenschaften |date=December 2000 |volume=87 |issue=11 |page=471 |doi=10.1007/s001140050762 |bibcode=2000NW.....87..467C }}</ref>  Ericoid mycorrhizae are only present in the Ericales order for plant hosts, and the Leotiales order of fungi.<ref>{{cite journal |last1=Cairney |first1=J.W.G. |title=Evolution of Mycorrhiza Systems |journal=Naturwissenschaften |date=December 2000 |volume=87 |issue=11 |page=473 |doi=10.1007/s001140050762 |bibcode=2000NW.....87..467C }}</ref>  This specialization suggests that ericoid mycorrhizal partners evolved in parallel with one another in response to environmental change, rather than through reciprocal species-to-species level selection.<ref>{{cite journal |last1=Cairney |first1=J.W.G. |title=Evolution of Mycorrhiza Systems |journal=Naturwissenschaften |date=December 2000 |volume=87 |issue=11 |page=473 |doi=10.1007/s001140050762 |bibcode=2000NW.....87..467C }}</ref>  

Ericoid mycorrhizal relationships are found in extremely nutrient poor soils in the northern and southern hemispheres.<ref>{{cite journal |last1=Cairney |first1=J.W.G. |title=Evolution of Mycorrhiza Systems |journal=Naturwissenschaften |date=December 2000 |volume=87 |issue=11 |page=471 |doi=10.1007/s001140050762 |bibcode=2000NW.....87..467C }}</ref>  These environments of low mineral nutrient availability have led to native plants developing sclerophylly, where plants become high in lignin and low in phosphorus and nitrogen.<ref>{{cite journal |last1=Cairney |first1=J.W.G. |title=Evolution of Mycorrhiza Systems |journal=Naturwissenschaften |date=December 2000 |volume=87 |issue=11 |page=471 |doi=10.1007/s001140050762 |bibcode=2000NW.....87..467C }}</ref>  As a result, decaying plant matter in these areas has an abnormally high carbon to nitrogen ratio, making it resistant to microbial decay. Ericoid mycorrhizae have apparently evolved to conserve minerals in nutrient deficient sclerophyllous litter by directly cycling these nutrients throughout the mycorrhiza system.<ref>{{cite journal |last1=Cairney |first1=J.W.G. |title=Evolution of Mycorrhiza Systems |journal=Naturwissenschaften |date=December 2000 |volume=87 |issue=11 |page=471 |doi=10.1007/s001140050762 |bibcode=2000NW.....87..467C }}</ref> Ericoid mycorrhizae also retain saprotrophic abilities, allowing them to extract nitrogen and phosphorus from unmineralized organic material, and resist negative outcomes from high concentrations of toxic cations in the acidic soil environment.<ref>{{cite journal |last1=Cairney |first1=J.W.G. |title=Evolution of Mycorrhiza Systems |journal=Naturwissenschaften |date=December 2000 |volume=87 |issue=11 |page=471 |doi=10.1007/s001140050762 |bibcode=2000NW.....87..467C }}</ref>