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Journal ArticleDOI

The C4 plant lineages of planet Earth

01 May 2011-Journal of Experimental Botany (Oxford University Press)-Vol. 62, Iss: 9, pp 3155-3169
TL;DR: Using isotopic screens, phylogenetic assessments, and 45 years of physiological data, it is now possible to identify most of the evolutionary lineages expressing the C(4) photosynthetic pathway, and is thus an outstanding system to study the mechanisms of evolutionary adaptation.
Abstract: Using isotopic screens, phylogenetic assessments, and 45 years of physiological data, it is now possible to identify most of the evolutionary lineages expressing the C 4 photosynthetic pathway. Here, 62 recognizable lineages of C 4 photosynthesis are listed. Thirty-six lineages (60%) occur in the eudicots. Monocots account for 26 lineages, with a minimum of 18 lineages being present in the grass family and six in the sedge family. Species exhibiting the C 3 ‐C 4 intermediate type of photosynthesis correspond to 21 lineages. Of these, 9 are not immediately associated with any C 4 lineage, indicating that they did not share common C 3 ‐C 4 ancestors with C 4 species and are instead an independent line. The geographic centre of origin for 47 of the lineages could be estimated. These centres tend to cluster in areas corresponding to what are now arid to semi-arid regions of southwestern North America, southcentral South America, central Asia, northeastern and southern Africa, and inland Australia. With 62 independent lineages, C 4 photosynthesis has to be considered one of the most convergent of the complex evolutionary phenomena on planet Earth, and is thus an outstanding system to study the mechanisms of evolutionary adaptation.

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Journal ArticleDOI
TL;DR: This paper features the first comprehensive and critical account of European syntaxa and synthesizes more than 100 yr of classification effort by European phytosociologists.
Abstract: Aims: Vegetation classification consistent with the Braun-Blanquet approach is widely used in Europe for applied vegetation science, conservation planning and land management. During the long history of syntaxonomy, many concepts and names of vegetation units have been proposed, but there has been no single classification system integrating these units. Here we (1) present a comprehensive, hierarchical, syntaxonomic system of alliances, orders and classes of Braun-Blanquet syntaxonomy for vascular plant, bryophyte and lichen, and algal communities of Europe; (2) briefly characterize in ecological and geographic terms accepted syntaxonomic concepts; (3) link available synonyms to these accepted concepts; and (4) provide a list of diagnostic species for all classes. LocationEuropean mainland, Greenland, Arctic archipelagos (including Iceland, Svalbard, Novaya Zemlya), Canary Islands, Madeira, Azores, Caucasus, Cyprus. Methods: We evaluated approximately 10000 bibliographic sources to create a comprehensive list of previously proposed syntaxonomic units. These units were evaluated by experts for their floristic and ecological distinctness, clarity of geographic distribution and compliance with the nomenclature code. Accepted units were compiled into three systems of classes, orders and alliances (EuroVegChecklist, EVC) for communities dominated by vascular plants (EVC1), bryophytes and lichens (EVC2) and algae (EVC3). Results: EVC1 includes 109 classes, 300 orders and 1108 alliances; EVC2 includes 27 classes, 53 orders and 137 alliances, and EVC3 includes 13 classes, 24 orders and 53 alliances. In total 13448 taxa were assigned as indicator species to classes of EVC1, 2087 to classes of EVC2 and 368 to classes of EVC3. Accepted syntaxonomic concepts are summarized in a series of appendices, and detailed information on each is accessible through the software tool EuroVegBrowser. Conclusions: This paper features the first comprehensive and critical account of European syntaxa and synthesizes more than 100 yr of classification effort by European phytosociologists. It aims to document and stabilize the concepts and nomenclature of syntaxa for practical uses, such as calibration of habitat classification used by the European Union, standardization of terminology for environmental assessment, management and conservation of nature areas, landscape planning and education. The presented classification systems provide a baseline for future development and revision of European syntaxonomy.

817 citations


Cites background from "The C4 plant lineages of planet Ear..."

  • ...C4 (plant): those plants using the C4-photosynthetic strategy to assimilate carbon dioxide (see Sage et al. 2011). dealpine (organism, vegetation): occurring in relict, post-glacial habitats, usually at lower altitudes at the periphery of high mountain ranges, retaining certain microclimatic…...

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Journal ArticleDOI
TL;DR: Phylogenetically informed research indicates that the repositioning of mitochondria in the bundle sheath is one of the earliest steps in C(4) evolution, as it may establish a single-celled mechanism to scavenge photorespired CO(2) produced in the bundles sheath cells.
Abstract: C(4) photosynthesis is one of the most convergent evolutionary phenomena in the biological world, with at least 66 independent origins. Evidence from these lineages consistently indicates that the C(4) pathway is the end result of a series of evolutionary modifications to recover photorespired CO(2) in environments where RuBisCO oxygenation is high. Phylogenetically informed research indicates that the repositioning of mitochondria in the bundle sheath is one of the earliest steps in C(4) evolution, as it may establish a single-celled mechanism to scavenge photorespired CO(2) produced in the bundle sheath cells. Elaboration of this mechanism leads to the two-celled photorespiratory concentration mechanism known as C(2) photosynthesis (commonly observed in C(3)-C(4) intermediate species) and then to C(4) photosynthesis following the upregulation of a C(4) metabolic cycle.

582 citations


Cites background from "The C4 plant lineages of planet Ear..."

  • ...occur in phylogenetic branches that are sister to C4 lineages, indicating potential ancestry; however, 9 are separate enough within a phylogeny to indicate no ancestry to C4 species (Table 1) (25, 118)....

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  • ...In total, 62 distinct lineages of C4 photosynthesis are listed in a recent survey (118)....

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  • ...The C4 pathway evolved independently at least 66 times within the past 35 million years, making it one of the best examples of evolutionary convergence in the living world (52, 118)....

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  • ...’s (118) study published in 2011, bringing the current number of known lineages to 66–68 (52)....

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  • ...Both genera have extant species that qualify as evolutionary intermediates between the C3 and C4 condition, with Flaveria having nine C3–C4 intermediate species (118)....

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Journal ArticleDOI
TL;DR: The effective use of Δ across its full range of applications will require a holistic view of the interplay between environmental control and physiological modulation of the environmental signal.
Abstract: Summary Stable carbon isotope ratios (d 13 C) of terrestrial plants are employed across a diverse range of applicationsinenvironmentalandplantsciences;however,thekindofinformationthatisdesired fromthed 13 Csignaloftendiffers.Attheextremes,itrangesbetweenpurely environmentaland purely biological. Here, we review environmental drivers of variation in carbon isotope discrimination (D) in terrestrial plants, and the biological processes that can either damp or amplifytheresponse.ForC3plants,whereDisprimarilycontrolledbytheratioofintercellularto ambient CO2 concentrations (ci/ca), coordination between stomatal conductance and photo- synthesisandleafareaadjustmenttendstoconstrainthepotentialenvironmentallydrivenrange of D. For C4 plants, variation in bundle-sheath leakiness to CO2 can either damp or amplify the effects of ci/ca on D. For plants with crassulacean acid metabolism (CAM), D varies over a relatively largerange asafunctionoftheproportion ofdaytimetonight-time CO2fixation. This range can be substantially broadened by environmental effects onD when carbon uptake takes place primarily during the day. The effective use of D across its full range of applications will require a holistic view of the interplay between environmental control and physiological modulation of the environmental signal.

471 citations


Cites background from "The C4 plant lineages of planet Ear..."

  • ...It occursmainly in grasses, in somedicotyledonous herbs, shrubs, and in a small number of trees (Pearcy & Troughton, 1975; Sage et al., 2011)....

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Journal ArticleDOI
TL;DR: The data demonstrate that Cd perturbs the DNA methylation status through the involvement of a specific methyltransferase, linked to nuclear chromatin reconfiguration likely to establish a new balance of expressed/repressed chromatin.
Abstract: In mammals, cadmium is widely considered as a non-genotoxic carcinogen acting through a methylation-dependent epigenetic mechanism. Here, the effects of Cd treatment on the DNA methylation patten are examined together with its effect on chromatin reconfiguration in Posidonia oceanica. DNA methylation level and pattern were analysed in actively growing organs, under short- (6 h) and long- (2 d or 4 d) term and low (10 mM) and high (50 mM) doses of Cd, through a Methylation-Sensitive Amplification Polymorphism technique and an immunocytological approach, respectively. The expression of one member of the CHROMOMETHYLASE (CMT) family, a DNA methyltransferase, was also assessed by qRT-PCR. Nuclear chromatin ultrastructure was investigated by transmission electron microscopy. Cd treatment induced a DNA hypermethylation, as well as an up-regulation of CMT, indicating that de novo methylation did indeed occur. Moreover, a high dose of Cd led to a progressive heterochromatinization of interphase nuclei and apoptotic figures were also observed after long-term treatment. The data demonstrate that Cd perturbs the DNA methylation status through the involvement of a specific methyltransferase. Such changes are linked to nuclear chromatin reconfiguration likely to establish a new balance of expressed/repressed chromatin. Overall, the data show an epigenetic basis to the mechanism underlying Cd toxicity in plants.

450 citations

Journal ArticleDOI
09 Nov 2018-Science
TL;DR: The authors' review of many such experiments indicates that responses across replicate populations are often repeatable to some degree, although divergence increases as analyses move from overall fitness to underlying phenotypes and genetic changes.
Abstract: Historical processes display some degree of "contingency," meaning their outcomes are sensitive to seemingly inconsequential events that can fundamentally change the future. Contingency is what makes historical outcomes unpredictable. Unlike many other natural phenomena, evolution is a historical process. Evolutionary change is often driven by the deterministic force of natural selection, but natural selection works upon variation that arises unpredictably through time by random mutation, and even beneficial mutations can be lost by chance through genetic drift. Moreover, evolution has taken place within a planetary environment with a particular history of its own. This tension between determinism and contingency makes evolutionary biology a kind of hybrid between science and history. While philosophers of science examine the nuances of contingency, biologists have performed many empirical studies of evolutionary repeatability and contingency. Here, we review the experimental and comparative evidence from these studies. Replicate populations in evolutionary "replay" experiments often show parallel changes, especially in overall performance, although idiosyncratic outcomes show that the particulars of a lineage's history can affect which of several evolutionary paths is taken. Comparative biologists have found many notable examples of convergent adaptation to similar conditions, but quantification of how frequently such convergence occurs is difficult. On balance, the evidence indicates that evolution tends to be surprisingly repeatable among closely related lineages, but disparate outcomes become more likely as the footprint of history grows deeper. Ongoing research on the structure of adaptive landscapes is providing additional insight into the interplay of fate and chance in the evolutionary process.

364 citations

References
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5,035 citations


"The C4 plant lineages of planet Ear..." refers background in this paper

  • ...The Amaranthaceae sensu lato (¼ Chenopodiaceae ss and Amaranthaceae ss; APG III, 2009) is the most prolific family, with 15 distinct lineages of C4 taxa and ;750 C4 species (Figs 1, 2; Sage et al., 1999)....

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  • ...APG III....

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  • ...An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG III....

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  • ...26 Caryophyllales Gisekiaceae Gisekia Unknown Unknown Old World APG III (2009) 27 Caryophyllales Molluginaceae Mollugo cerviana/...

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  • ...Because they are the only known C4 representatives of broader and presumably monophyletic taxonomic groups whose phylogenetic positions have been determined (APG III, 2009), they are reported as distinct C4 lineages....

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Journal ArticleDOI
TL;DR: δ 13C/12C ratios have been determined for plant tissue from 104 species representing 60 families and photosynthetic fractionation leading to such values is discussed.
Abstract: 13C/12C ratios have been determined for plant tissue from 104 species representing 60 families. Higher plants fall into two categories, those with low δPDBI13C values (—24 to —34‰) and those with high δ 13C values (—6 to —19‰). Algae have δ 13C values of —12 to —23‰. Photosynthetic fractionation leading to such values is discussed.

1,943 citations


"The C4 plant lineages of planet Ear..." refers background in this paper

  • ...With this comprehensive understanding, plant biologists were able to survey the plant kingdom rapidly and by the mid-1970s identified most of the genera containing C4 species (Smith and Epstein, 1971; Downton, 1975; Smith and Turner, 1975; Webster et al., 1975; Sankhla et al., 1975)....

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Journal ArticleDOI
TL;DR: Gene duplication followed by neo- and nonfunctionalization are the leading mechanisms for creating C4 genomes, with selection for carbon conservation traits under conditions promoting high photorespiration being the ultimate factor behind the origin of C4 photosynthesis.
Abstract: Contents Summary 341 I. Introduction 342 II. What is C4 photosynthesis? 343 III. Why did C4 photosynthesis evolve? 347 IV. Evolutionary lineages of C4 photosynthesis 348 V. Where did C4 photosynthesis evolve? 350 VI. How did C4 photosynthesis evolve? 352 VII. Molecular evolution of C4 photosynthesis 361 VIII. When did C4 photosynthesis evolve 362 IX. The rise of C4 photosynthesis in relation to climate and CO2 363 X. Final thoughts: the future evolution of C4 photosynthesis 365 Acknowledgements 365 References 365 Summary C4 photosynthesis is a series of anatomical and biochemical modifications that concentrate CO2 around the carboxylating enzyme Rubisco, thereby increasing photosynthetic efficiency in conditions promoting high rates of photorespiration. The C4 pathway independently evolved over 45 times in 19 families of angiosperms, and thus represents one of the most convergent of evolutionary phenomena. Most origins of C4 photosynthesis occurred in the dicots, with at least 30 lineages. C4 photosynthesis first arose in grasses, probably during the Oligocene epoch (24–35 million yr ago). The earliest C4 dicots are likely members of the Chenopodiaceae dating back 15–21 million yr; however, most C4 dicot lineages are estimated to have appeared relatively recently, perhaps less than 5 million yr ago. C4 photosynthesis in the dicots originated in arid regions of low latitude, implicating combined effects of heat, drought and/or salinity as important conditions promoting C4 evolution. Low atmospheric CO2 is a significant contributing factor, because it is required for high rates of photorespiration. Consistently, the appearance of C4 plants in the evolutionary record coincides with periods of increasing global aridification and declining atmospheric CO2. Gene duplication followed by neo- and nonfunctionalization are the leading mechanisms for creating C4 genomes, with selection for carbon conservation traits under conditions promoting high photorespiration being the ultimate factor behind the origin of C4 photosynthesis.

1,057 citations


"The C4 plant lineages of planet Ear..." refers background or methods in this paper

  • ...The literature was screened for taxonomic surveys of photosynthetic types as well as phylogenetic information, and then the occurrence of C4 photosynthesis was mapped onto recent phylogenies following the approach of Kellogg (1999) and Sage (2004)....

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  • ...Following the mutation leading to GDC localization, C3–C4 species evolve many C4-like traits such as close vein spacing and enlarged BSCs to optimize the efficiency of photorespiratory CO2 concentration (Sage, 2004)....

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  • ...This compares with 45 lineages listed by Sage (2004) and 31 listed by Kellogg (1999)....

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  • ...…is that reduction in atmospheric CO2 in the late Oligocene increased photorespiration in warm climates, thereby facilitating selection for CO2-concentrating mechanisms such as C4 photosynthesis (Sage, 2001, 2004; Christin et al., 2008; Vicentini et al., 2009; Edwards et al., 2010; Osborne, 2011)....

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  • ...Anatomical characters in C3 ancestors could include close vein spacing, enlarged BSCs, or low mesophyll to bundle sheath ratios (Sage, 2004; McKown et al., 2005; Sage et al., 2011)....

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Journal ArticleDOI
30 Apr 2010-Science
TL;DR: A synthesis of grass evolutionary biology with grassland ecosystem science will further knowledge of the evolution of traits that promote dominance in grassland systems and will provide a new context in which to evaluate the relative importance of C4 photosynthesis in transforming ecosystems across large regions of Earth.
Abstract: The evolution of grasses using C4 photosynthesis and their sudden rise to ecological dominance 3 to 8 million years ago is among the most dramatic examples of biome assembly in the geological record. A growing body of work suggests that the patterns and drivers of C4 grassland expansion were considerably more complex than originally assumed. Previous research has benefited substantially from dialog between geologists and ecologists, but current research must now integrate fully with phylogenetics. A synthesis of grass evolutionary biology with grassland ecosystem science will further our knowledge of the evolution of traits that promote dominance in grassland systems and will provide a new context in which to evaluate the relative importance of C4 photosynthesis in transforming ecosystems across large regions of Earth.

878 citations


"The C4 plant lineages of planet Ear..." refers background in this paper

  • ...…is that reduction in atmospheric CO2 in the late Oligocene increased photorespiration in warm climates, thereby facilitating selection for CO2-concentrating mechanisms such as C4 photosynthesis (Sage, 2001, 2004; Christin et al., 2008; Vicentini et al., 2009; Edwards et al., 2010; Osborne, 2011)....

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