Arbuscular mycorrhizal‐like fungi in Carboniferous arborescent lycopsids

Krings, Michael; Taylor, Thomas N.; Taylor, Edith L.; Dotzler, Nora; Walker, Christopher

doi:10.1111/j.1469-8137.2011.03752.x

Cited by 36 publications

(22 citation statements)

References 23 publications

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“…Recent studies have built on this foundation of knowledge and have shed fresh light on physiological mechanism controlling their development, structure, and interaction with other organisms (63)(64)(65)(66). The discovery that stigmarian rootlets were highly branched, developed root hairs and share the same branching architecture as extant Isoetes rootlets reveals a remarkable conservatism in rootlet architecture between the first giant trees and their only living herbaceous relatives.…”

Section: Discussionmentioning

confidence: 99%

Networks of highly branched stigmarian rootlets developed on the first giant trees

Hetherington

Berry

Dolan

2016

Proc. Natl. Acad. Sci. U.S.A.

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Lycophyte trees, up to 50 m in height, were the tallest in the Carboniferous coal swamp forests. The similarity in their shoot and root morphology led to the hypothesis that their rooting (stigmarian) systems were modified leafy shoot systems, distinct from the roots of all other plants. Each consists of a branching main axis covered on all sides by lateral structures in a phyllotactic arrangement; unbranched microphylls developed from shoot axes, and largely unbranched stigmarian rootlets developed from rhizomorphs axes. Here, we reexamined the morphology of extinct stigmarian systems preserved as compression fossils and in coal balls from the Carboniferous period. Contrary to the long-standing view of stigmarian systems, where shoot-like rhizomorph axes developed largely unbranched, root-hairless rootlets, here we report that stigmarian rootlets were highly branched, developed at a density of ∼25,600 terminal rootlets per meter of rhizomorph, and were covered in root hairs. Furthermore, we show that this architecture is conserved among their only extant relatives, herbaceous plants in the Isoetes genus. Therefore, despite the difference in stature and the time that has elapsed, we conclude that both extant and extinct rhizomorphic lycopsids have the same rootlet system architecture.evolution | paleobotany | Carboniferous forests | stigmarian root systems | Isoetes T he spread of the first wetland forests with tall trees during the Carboniferous period (359-300 million years ago) had a dramatic impact on the carbon cycle by burying large amounts of organic carbon in the form of peat in coal swamps (1, 2). Lycophyte trees up to 50 m in height (3, 4) were dominant components of coal swamp forests (5, 6). They were key components of coal-forming environments throughout the Carboniferous period but dominated in the lower-middle Pennsylvanian (Namurian-Wetsphalian) where they typically contribute between 60% and 95% of the biomass in buried peat (7-13). The preserved remains of lycophyte trees form some of the most extensive fossil plant deposits of any geological period. This is in part because of their size and ecological dominance but also the result of the high probability of preservation in the waterlogged conditions in which these trees grew (4). Detailed descriptions of the morphology of these plants on a range of scales-from entire in situ tree lycophyte forests (14, 15) to cellular descriptions of developing spores (16)-have made these trees some of the best understood fossil plants of the Carboniferous coal swamps.The rooting system of the arborescent lycopsids-stigmarian systems-consist of large shoot-like axes (rhizomorphs) that develop lateral organs called rootlets (4,(17)(18)(19)(20). Rootlets, which have been described as largely unbranched and root hairless (4,5,(17)(18)(19)(20)(21)(22)(23)(24), are arranged in a characteristic pattern or rhizotaxy on the rhizomorph (25). It is the arrangement of these largely unbranched leaf-like rootlets on a shoot-like axis that first led to the theory that stigm...

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Section: Discussionmentioning

confidence: 99%

Networks of highly branched stigmarian rootlets developed on the first giant trees

Hetherington

Berry

Dolan

2016

Proc. Natl. Acad. Sci. U.S.A.

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“…Krings et al (2011) reported an AM-like fungus in the root system of an arborescent clubmoss from the latter part of the Carboniferous Period (315 million years ago). These plants bore an extensive root system with a unique evolutionary history.…”

Section: Fungal Partnershipsmentioning

confidence: 99%

The Origin and Early Evolution of Roots

2014

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Geological sites of exceptional fossil preservation are becoming a focus of research on root evolution because they retain edaphic and ecological context, and the remains of plant soft tissues are preserved in some. New information is emerging on the origins of rooting systems, their interactions with fungi, and their nature and diversity in the earliest forest ecosystems. Remarkably wellpreserved fossils prove that mycorrhizal symbionts were diverse in simple rhizoid-based systems. Roots evolved in a piecemeal fashion and independently in several major clades through the Devonian Period (416 to 360 million years ago), rapidly extending functionality and complexity. Evidence from extinct arborescent clades indicates that polar auxin transport was recruited independently in several to regulate wood and root development. The broader impact of root evolution on the geochemical carbon cycle is a developing area and one in which the interests of the plant physiologist intersect with those of the geochemist.

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“…However, some liverworts host fungal glomeralean endophytes (Chambers et al, 1999;Davis et al, 2003) that probably serve mutualistic rather than parasitic roles. Similarly, some modern lycopods host glomeralean endophytes (Read et al, 2000;Winther and Friedman, 2007) that form associations extending deep into the Paleozoic permineralized record Krings et al, 2005;Krings et al, 2007;Krings et al, 2011). Like lycopods, horsetails possess few diseases (Freeberg, 1962), except for a variety of maladies that affect silica metabolism (Ellis and Ellis, 1985;Quarles, 1995;Epstein, 1999), and especially bacterioses that are induced by strains of Pseudomonas syringae that afflict wheat and secondarily target Equisetum (Pasichnik et al, 2012).…”

Section: Can Plant Diseases Be Recognized In the Preangiospermous Fosmentioning

confidence: 99%

“…A difficulty in interpreting the presence of a fungal or other potential pathogen within host tissues is that the host likely was dead when it was preserved, and was exposed to the effects of non-pathogenic, saprophytic organisms. In addition, while alive, the plant may have hosted endophytic fungi that did not elicit a disease response (Krings et al, 2009(Krings et al, , 2011 and cannot be considered unequivocally as having been pathogenic, despite its presence within the tissues of the plant. Only the clear presence of a host reaction to an invading organism, or the presence of specialized hyphae such as haustoria that are known to be adaptations of an obligately biotrophic mode of life, are considered here to be adequate evidence for an observed pathogenic interaction.…”

Section: An Overview Of Pathogens In the Permineralized Fossil Recordmentioning

confidence: 99%

Plant paleopathology and the roles of pathogens and insects

Labandeira

Prevec

2014

International Journal of Paleopathology

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Arbuscular mycorrhizal‐like fungi in Carboniferous arborescent lycopsids

Abstract: Arbuscular mycorrhizal (AM)-like fungi in stigmarian appendagesStructurally preserved stigmarian appendages containing an AM-like endophytic fungus have been discovered in thinsection preparations of coal ball material from the Carboniferous of Great Britain.

Cited by 36 publications

References 23 publications

Networks of highly branched stigmarian rootlets developed on the first giant trees

Networks of highly branched stigmarian rootlets developed on the first giant trees

The Origin and Early Evolution of Roots

Plant paleopathology and the roles of pathogens and insects

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