John C Cushman

University of Nevada, Reno, Reno, Nevada, United States

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Publications (123)563.79 Total impact

  • [Show abstract] [Hide abstract]
    ABSTRACT: Global climate change threatens the sustainability of agriculture and agroforestry worldwide through increased heat, drought, surface evaporation, and associated soil drying. Exposure of crops and forests to warmer and drier environments will increase leaf:air water vapor-pressure deficits (VPD), and result in increased drought susceptibility and reduced productivity, particularly in arid regions, but also in tropical regions with seasonal dry periods. Fast-growing, short-rotation forestry (SRF) bioenergy crops such, as poplar (Populus spp.) and willow (Salix spp.), are particularly susceptible to hydraulic failure following drought stress due to their isohydric nature and relatively high stomatal conductance. One approach to sustaining plant productivity is to improve water-use efficiency (WUE) by engineering crassulacean acid metabolism (CAM) into C3 crops. CAM improves WUE by shifting stomatal opening and primary CO2 uptake and fixation to the nighttime when leaf:air VPD is low. CAM members of the tree genus Clusia exemplify the compatibility of CAM performance within tree species and highlight CAM as a mechanism to conserve water and maintain carbon uptake during drought conditions. The introduction of bioengineered CAM into SRF bioenergy trees is a potentially viable path to sustaining agroforestry production systems in the face of a globally changing climate.
    Plant Cell and Environment 11/2014; · 5.91 Impact Factor
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    ABSTRACT: Crassulacean acid metabolism (CAM) is an elaboration of C3 photosynthesis wherein carbon assimilation occurs at night to reduce daytime water losses through a temporal separation of primary C4 and secondary C3 carboxylation reactions. The circadian clock controls the temporal separation of these potentially competing reactions. However, the underlying orchestration of transcriptional network modules of CAM is poorly understood. Comparative RNA-seq analysis was performed in well-watered (C3 performing) and water-deficit-stressed (CAM performing) common ice plants (Mesembryanthemum crystallinum L.), a facultative CAM model species. Leaves were collected every 4 h over a 72 h time course under both 24 h light/dark and 48 h light/light conditions to characterize the circadian clock-controlled transcriptome in both the C3 photosynthesis and CAM states. Under water-deficit conditions that induce CAM, greater numbers of transcripts become rhythmic indicating that the stress-adaptive and CAM transcriptional machinery is directly under circadian clock control. Weighted co-expression network analyses of differentially expressed genes upon CAM induction (log2 fold-change in CAM performing compared to C3 photosynthesis performing) revealed both persistent and induced circadian clock-controlled transcriptional network modules. Together these results tentatively identified CAM-specific network modules and provide insights into the circadian clock controlled transcriptional expression of CAM.
    34th New Phytologist Symposium: Systems Biology and Ecology of CAM plants, Lake Tahoe, CA; 07/2014
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    ABSTRACT: Phosphoenolpyruvate carboxylase (PEPC) catalyses the initial fixation of atmospheric CO2 into oxaloacetate and subsequently malate. Nocturnal accumulation of malic acid within the vacuole of photosynthetic cells is a typical feature of plants that perform crassulacean acid metabolism (CAM). PEPC is a ubiquitous plant enzyme encoded by a small gene family, and each member encodes an isoform with specialized function. CAM-specific PEPC isoforms probably evolved from ancestral non-photosynthetic isoforms by gene duplication events and subsequent acquisition of transcriptional control elements that mediate increased leaf-specific or photosynthetic-tissue-specific mRNA expression. To understand the patterns of functional diversification related to the expression of CAM, ppc gene families and photosynthetic patterns were characterized in 11 closely related orchid species from the subtribe Oncidiinae with a range of photosynthetic pathways from C3 photosynthesis (Oncidium cheirophorum, Oncidium maduroi, Rossioglossum krameri, and Oncidium sotoanum) to weak CAM (Oncidium panamense, Oncidium sphacelatum, Gomesa flexuosa and Rossioglossum insleayi) and strong CAM (Rossioglossum ampliatum, Trichocentrum nanum, and Trichocentrum carthagenense). Phylogenetic analysis revealed the existence of two main ppc lineages in flowering plants, two main ppc lineages within the eudicots, and three ppc lineages within the Orchidaceae. Our results indicate that ppc gene family expansion within the Orchidaceae is likely to be the result of gene duplication events followed by adaptive sequence divergence. CAM-associated PEPC isoforms in the Orchidaceae probably evolved from several independent origins.
    Journal of Experimental Botany 06/2014; · 5.79 Impact Factor
  • John C Cushman
    Trends in Plant Science 04/2014; · 13.48 Impact Factor
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    ABSTRACT: To meet future food and energy security needs, which are amplified by increasing population growth and reduced natural resource availability, metabolic engineering efforts have moved from manipulating single genes/proteins to introducing multiple genes and novel pathways to improve photosynthetic efficiency in a more comprehensive manner. Biochemical carbon-concentrating mechanisms such as crassulacean acid metabolism (CAM), which improves photosynthetic, water-use, and possibly nutrient-use efficiency, represent a strategic target for synthetic biology to engineer more productive C3 crops for a warmer and drier world. One key challenge for introducing multigene traits like CAM onto a background of C3 photosynthesis is to gain a better understanding of the dynamic spatial and temporal regulatory events that underpin photosynthetic metabolism. With the aid of systems and computational biology, vast amounts of experimental data encompassing transcriptomics, proteomics, and metabolomics can be related in a network to create dynamic models. Such models can undergo simulations to discover key regulatory elements in metabolism and suggest strategic substitution or augmentation by synthetic components to improve photosynthetic performance and water-use efficiency in C3 crops. Another key challenge in the application of synthetic biology to photosynthesis research is to develop efficient systems for multigene assembly and stacking. Here, we review recent progress in computational modelling as applied to plant photosynthesis, with attention to the requirements for CAM, and recent advances in synthetic biology tool development. Lastly, we discuss possible options for multigene pathway construction in plants with an emphasis on CAM-into-C3 engineering.
    Journal of Experimental Botany 02/2014; · 5.79 Impact Factor
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    ABSTRACT: Climatic extremes threaten agricultural sustainability worldwide. One approach to increase plant water- use efficiency (WUE) is to introduce crassulacean acid metabolism (CAM) into C3 crops. Such a task requires comprehensive systems-level understanding of the enzymatic and regulatory pathways underpinning this temporal CO2 pump. Here we review the progress that has been made in achieving this goal. Given that CAM arose through multiple independent evolutionary ori- gins, comparative transcriptomics and genomics of taxonomically diverse CAM species are being used to define the genetic ‘parts list’ required to operate the core CAM functional modules of nocturnal carboxylation, diurnal decarboxylation, and inverse stomatal regulation. Engi- neered CAM offers the potential to sustain plant productivity for food, feed, fiber, and biofuel production in hotter and drier climates.
    Trends in Plant Science 02/2014; 19(6). · 13.48 Impact Factor
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    ABSTRACT: Improved crop water-use efficiency (WUE) is critical for the long-term sustainability of agricultural production systems in the face of predicted future warmer and drier climates. Crassulacean acid metabolism (CAM) is a specialized mode of photosynthesis that enhances WUE through an inverse day/night pattern of stomatal closure/opening and improves photosynthetic efficiency by concentrating CO2 around RUBISCO. CAM has evolved multiple times from C3 photosynthesis and ~6.5% of higher plant species in more than 35 families have acquired CAM via parallel or convergent evolution. There are two fundamental questions to be answered to understand the molecular basis and evolutionary mechanism of CAM: 1) what are the genetic differences between CAM and non-CAM species and 2) what are the common molecular features shared among CAM plants from diverse origins? To address these questions, comparative genomics analysis was performed using multiple plant species including CAM (e.g., Agave, Kalanchoe, Mesembryanthemum), C3 (e.g., Arabidopsis, Oryza, Populus), C4 (e.g., Setaria, Sorghum, and Zea), and non-vascular plant species (e.g., Physcomitrella, Selaginella). Our analysis not only revealed orthologous gene groups shared between CAM and non-CAM species, but also identified genes specific to the CAM species. Also, expanded gene families were identified in CAM species compared with non-CAM species. Gene ontology and gene expression profiles were used to build hypothesis related to divergent gene functions that likely arose during CAM evolution. This research establishes a framework for CAM comparative genomics studies and provides new knowledge to inform genetic improvement in WUE and photosynthetic efficiency in crop plants under water-limiting conditions.
    International Plant and Animal Genome Conference XXII 2014; 01/2014
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    ABSTRACT: Crassulacean acid metabolism (CAM) is a water-use efficient photosynthetic adaptation found in more than 6% of vascular plant species. This adaptation is distinguished by the temporal separation of primary C4 and secondary C3 carboxylation reactions to reduce daytime water loss. To investigate the underlying orchestration of transcriptional networks controlling the temporal separation of these competing carboxylation reactions and their associated metabolic demands, transcriptomic and metabolomic analyses were conducted on the facultative CAM ice plant, Mesembryanthemum crystallinum. These omic technologies revealed diel and circadian changes in transcript and metabolite abundance patterns in ice plants performing C3 and CAM (induced by water-deficit stress) over a 72 h time course. Key differences in transcripts and metabolites were identified between the C3 and CAM states that are involved in CAM adaptation and possibly their role in the regulation of CAM by the circadian clock. Other pivotal omic results and candidate CAM transcription factors to elucidate clock-controlled regulatory networks operating in mesophyll cells will be discussed.
    International Plant and Animal Genome Conference XXII 2014; 01/2014
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    ABSTRACT: Crassulacean acid metabolism (CAM) is an elaboration of C3 photosynthetic that limits atmospheric CO2 fixation to all or part of the nighttime thereby reducing transpiration during the day and improving water-use efficiency. The common or crystalline ice plant (Mesembryanthemum crystallinum L.) is a facultative CAM and halophytic model species that can switch from C3 photosynthesis to CAM following high salinity or water-deficit stress treatments. The estimated genome size of ice plant is 390 Mb in 9 chromosomes (2N=18). To reveal the molecular basis of halophytism and CAM, the ice plant genome is being sequenced and analyzed through hybrid assembly approaches. Results from three different sequencing platforms, Illumina Mate Pair (MP), Illumina Paired End (PE) and PacBio (PB) long reads, that are being used to sequence the genome will be discussed. Two strategies will be applied for hybrid assembly of the genome. Strategy 1 will build contigs from PB reads after error-correction by PE data followed by scaffolding using MP reads. Strategy 2 will rely on the assembly of contigs build from PE reads combined with scaffold assembly using MP reads, followed by gap filling with PB reads. The completed ice plant genome sequence will facilitate our understanding of the genomic basis of salt tolerance and the water-use efficiency that permits CAM species to inhabit semi-arid and arid environments.
    International Plant and Animal Genome Conference XXII 2014; 01/2014
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    ABSTRACT: The development of low water input forages would be useful for improving the water-use efficiency of livestock production in semi-arid and arid regions. The desiccation-tolerant (DT) species Sporobolus stapfianus Gandoger and two desic- cation-sensitive (DS) species, Sporobolus pyramidalis and Sporobolus fimbriatus (Trin.) Nees. (Poaceae), were evaluated for aerial biomass production and seed productivity under three different irrigation regimes. Sporobolus stapfianus dis- played the least biomass production, whereas S. pyramidalis and S. fimbriatus produced up to 3.8- and 11.2-fold greater dry biomass, respectively, at the highest irrigation rate of 12 334 l (0.01 acre-feet). Sporobolus fimbriatus and to a lesser extent S. pyramidalis showed significant increases in biomass production in response to increased irrigation rates, whereas S. stapfianus did not. Sporobolus pyramidalis and S. fimbriatus exhibited 3.2- and 6.0-fold greater seed production, respectively, in response to increased irrigation rates, whereas S. stapfianus showed only a 1.4-fold increase. All Sporobolus species possessed forage quality traits (e.g. crude protein, fibre content) comparable to those of timothy, a forage grass grown widely in the Great Basin in the western United States. Micronutrient content exceeded the minimum requirements of beef cattle, without surpassing tolerable limits, with the exception of zinc, which appeared low in all three Sporo- bolus species. The low water requirements displayed by these species, combined with their acceptable forage qualities, indicate that these grasses have the poten- tial to serve farmers and ranchers in semi-arid and arid regions of the western United States where irrigation resources are limited.
    Journal of Agronomy and Crop Science 10/2013; · 2.62 Impact Factor
  • International Symposium on C4 and CAM Plant Biology. Champaign, IL; 07/2013
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    ABSTRACT: Over 13% of all genes in the Arabidopsis thaliana genome encode for proteins classified as having a completely unknown function, with the function of >30% of the Arabidopsis proteome poorly characterized. Although empirical data in the form of mRNA and proteome profiling experiments suggest that many of these proteins play an important role in different biological processes, their functional characterization remains one of the major challenges in modern biology. To expand the annotation of genes with unknown function involved in the response of Arabidopsis to different environmental stress conditions, we selected 1007 such genes and tested the response of their corresponding homozygous T-DNA insertional mutants to salinity, oxidative, osmotic, heat, cold and hypoxia stresses. Depending on the specific abiotic stresses tested, 12-31% of mutants had an altered stress-response phenotype. Interestingly, 832 out of 1007 mutants showed tolerance or sensitivity to more than one abiotic stress treatment, suggesting that genes of unknown function could play an important role in abiotic stress-response signaling, or general acclimation mechanisms. Further analysis of multiple stress-response phenotypes within different populations of mutants revealed interesting links between acclimation to heat, cold and oxidative stresses, as well as between sensitivity to ABA, osmotic, salinity, oxidative and hypoxia stresses. Our findings provide a significant contribution to the biological characterization of genes with unknown function in Arabidopsis and demonstrate that many of these genes play a key role in the response of plants to abiotic stresses.
    Physiologia Plantarum 03/2013; · 3.26 Impact Factor
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    ABSTRACT: Aerobic metabolism of vertebrates is linked to membrane fatty acid (FA) composition. Although the membrane pacemaker hypothesis posits that desaturation of FAs accounts for variation in resting or basal metabolic rate (BMR), little is known about the FA profiles that underpin variation in maximal metabolic rate (MMR). We examined membrane FA composition of liver and skeletal muscle in mice after seven generations of selection for increased MMR. In both liver and skeletal muscle, unsaturation index did not differ between control and high-MMR mice. We also examined membrane FA composition at the individual-level of variation. In liver, 18:0, 20:3 n-6, 20:4 n-6, and 22:6 n-3 FAs were significant predictors of MMR. In gastrocnemius muscle, 18:2 n-6, 20:4 n-6, and 22:6 n-3 FAs were significant predictors of MMR. In addition, muscle 16:1 n-7, 18:1 n-9, and 22:5 n-3 FAs were significant predictors of BMR, whereas no liver FAs were significant predictors of BMR. Our findings indicate that (i) individual variation in MMR and BMR appears to be linked to membrane FA composition in the skeletal muscle and liver, and (ii) FAs that differ between selected and control lines are involved in pathways that can affect MMR or BMR.
    Comparative biochemistry and physiology. Part A, Molecular & integrative physiology 02/2013; · 2.20 Impact Factor
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    ABSTRACT: Selaginella lepidophylla is one of only a few species of spike mosses (Selaginellaceae) that have evolved desiccation tolerance (DT) or the ability to 'resurrect' from an air-dried state. In order to understand the metabolic basis of DT, S. lepidophylla was subjected to a five-stage, rehydration/dehydration cycle, then analyzed using non-biased, global metabolomics profiling technology based on GC/MS and UHLC/MS/MS2 platforms. A total of 251 metabolites including 167 named (66.5%) and 84 (33.4%) unnamed compounds were characterized. Only 42 (16.7%) and 74 (29.5%) of compounds showed significantly increased or decreased abundance, respectively, indicating that most compounds were produced constitutively including highly abundant trehalose, sucrose, and glucose. Several glycolysis/ gluconeogenesis and tricarboxylic acid (TCA) cycle intermediates showed increased abundance at 100% relative water content (RWC) and 50% RWC. Vanillate, a potent antioxidant was also more abundant in the hydrated state. Many different sugar alcohols and sugar acids were more abundant in the hydrated state. These polyols likely decelerate the rate of water loss during the drying process as well as slow water absorption during rehydration, stabilize proteins, and scavenge reactive oxygen species (ROS). In contrast, nitrogen-rich and γ-glutamyl amino acids, citrulline and nucleotide catabolism products (e.g., allantoin) were more abundant in the dry states, suggesting that these compounds might play important roles in nitrogen remobilization during rehydration or in ROS scavenging. UV-protective compounds such as 3-(3-hydroxyphenyl)propionate, apigenin and naringenin, were more abundant in the dry states. Most lipids were produced constitutively with the exception of choline phosphate, which likely plays a role in membrane hydration and stabilization. In contrast, several polyunsaturated fatty acids were more abundant in the hydrated states, suggesting that these compounds likely help maintain membrane fluidity during dehydration. Lastly, S. lepidophylla contained 7 unnamed compounds that displayed 2-fold or greater abundance in dry or rehydrating states, suggesting that these compounds might play adaptive roles in DT.
    Molecular Plant 12/2012; · 6.61 Impact Factor
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    ABSTRACT: Spike mosses (Selaginellaceae) represent an ancient lineage of vascular plants in which some species have evolved desiccation tolerance (DT). A sister-group contrast to reveal the metabolic basis of DT was conducted between a desiccation-tolerant species, Selaginella lepidophylla, and a desiccation-sensitive species, Selaginella moellendorffii, at 100% relative water content (RWC) and 50% RWC using non-biased, global metabolomics profiling technology, based on GC/MS and UHLC/MS/MS(2) platforms. A total of 301 metabolites, including 170 named (56.5%) and 131 (43.5%) unnamed compounds, were characterized across both species. S.  lepidophylla retained significantly higher abundances of sucrose, mono- and polysaccharides, and sugar alcohols than did S. moellendorffii. Aromatic amino acids, the well-known osmoprotectant betaine and flavonoids were also more abundant in S. lepidophylla. Notably, levels of γ-glutamyl amino acid, linked with glutathione metabolism in the detoxification of reactive oxygen species, and with possible nitrogen remobilization following rehydration, were markedly higher in S. lepidophylla. Markers for lipoxygenase activity were also greater in S. lepidophylla, especially at 50% RWC. S. moellendorffii contained more than twice the number of unnamed compounds, with only a slightly greater abundance than in S. lepidophylla. In contrast, S. lepidophylla contained 14 unnamed compounds of fivefold or greater abundance than in S. moellendorffii, suggesting that these compounds might play critical roles in DT. Overall, S. lepidophylla appears poised to tolerate desiccation in a constitutive manner using a wide range of metabolites with some inducible components, whereas S. moellendorffii mounts only limited metabolic responses to dehydration stress.
    The Plant Journal 10/2012; · 6.82 Impact Factor
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    ABSTRACT: Isolation of high quality, high molecular weight RNA from plant tissues is complicated by high levels of polyphenols and polysaccharides which bind to and/or co-precipitate with RNA. Using high molecular weight polyethylene glycol (HMW-PEG), RNA was successfully isolated from plant species in which other RNA extraction methods and commercially available kits failed to deliver suitable results. We tested various buffer systems and isolation conditions with and without PEG or PVP (polyvinylpyrrolidone) using tissue from species ofAloe, Ananas, Clusia, Euphorbia, Kalanchoe, Opuntia, andPyrrosia, all of which contain high amounts of phenolic compounds and/or polysaccharides. HMW-PEG was found to be more effective than PVP in removing these compounds. RNA extraction using HMW-PEG resulted in RNA of high quality from all species investigated, as indicated by UV light absorption profiles, and also yielded PCR amplification products after reverse transcription.
    Plant Molecular Biology Reporter 04/2012; 18(4):369-376. · 2.37 Impact Factor
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    ABSTRACT: In the halophytic species Mesembryanthemum crystallinum, the induction of crassulacean acid metabolism (CAM) by salinity requires a substantial investment of resources in storage carbohydrates to provide substrate for nocturnal CO(2) uptake. Acclimation to salinity also requires the synthesis and accumulation of cyclitols as compatible solutes, maintenance of root respiration, and nitrate assimilation. This study assessed the hierarchy and coordination of sinks for carbohydrate in leaves and roots during acclimation to salinity in M. crystallinum. By comparing wild type and a CAM-/starch-deficient mutant of this species, it was sought to determine if other metabolic sinks could compensate for a curtailment in CAM and enable acclimation to salinity. Under salinity, CAM deficiency reduced 24 h photosynthetic carbon gain by >50%. Cyclitols were accumulated to comparable levels in leaves and roots of both the wild type and mutant, but represented only 5% of 24 h carbon balance. Dark respiration of leaves and roots was a stronger sink for carbohydrate in the mutant compared with the wild type and implied higher maintenance costs for the metabolic processes underpinning acclimation to salinity when CAM was curtailed. CAM required the nocturnal mobilization of >70% of primary carbohydrate in the wild type and >85% of carbohydrate in the mutant. The substantial allocation of carbohydrate to CAM limited the export of sugars to roots, and the root:shoot ratio declined under salinity. The data suggest a key role for the vacuole in regulating the supply and demand for carbohydrate over the day/night cycle in the starch-/CAM-deficient mutant.
    Journal of Experimental Botany 01/2012; 63(5):1985-96. · 5.79 Impact Factor
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    ABSTRACT: To assess the suitability of microalgal strains for biodiesel production the lipid content and composition, especially individual triacylglycerols (TAG) and free fatty acids (FFA) must be determined. In this study, the compositions and concentrations of TAG and FFA were analysed in four halophytic algal species, Dunaliella salina, D. tertiolecta, D. bardawil, and D. granulata. These species were selected as part of a larger screen to identify species suitable for biofuel feedstocks. An accelerated solvent extraction instrument was used for lipids and fatty acid extraction using a dichloromethane–hexane solvent system. Ultra-performance liquid chromatography coupled with mass spectrometry (MS) detection was optimized and applied to the quantitative analysis of TAG and FFA in the different algal extracts. Individual TAG were characterized structurally using direct electrospray ionization (ESI) MS and MS/MS techniques. Cationic adducts (NH4+) of TAG were detected and quantified in the positive ESI MS and MS/MS modes, while the negative ESI mode was used for FFA analysis. Over 20 TAG were identified and quantified in the four Dunaliella strains. Analysis of FFA compositions demonstrated that the most abundant FFA in these four algal species were palmitic, linolenic, linoleic, and oleic acids.
    Journal of Oil & Fat Industries 01/2012; 90(1). · 1.62 Impact Factor
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    ABSTRACT: The capture and utilization of light is an exquisitely evolved process. The single-component microbial opsins, although more limited than multicomponent cascades in processing, display unparalleled compactness and speed. Recent advances in understanding microbial opsins have been driven by molecular engineering for optogenetics and by comparative genomics. Here we provide a Primer on these light-activated ion channels and pumps, describe a group of opsins bridging prior categories, and explore the convergence of molecular engineering and genomic discovery for the utilization and understanding of these remarkable molecular machines.
    Cell 12/2011; 147(7):1446-57. · 31.96 Impact Factor
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    ABSTRACT: Phylogenetic relationships within the orchid subtribe Oncidiinae sensu Chase were inferred using maximum likelihood analyses of single and multilocus DNA sequence data sets. Analyses included both nuclear ribosomal internal transcribed spacer DNA and plastid regions (matK exon, trnH-psbA intergenic spacer and two portions of ycf1 exon) for 736 individuals representing approximately 590 species plus seven outgroup taxa. Based on the well resolved and highly supported results, we recognize 61 genera in Oncidiinae. Mimicry of oil-secreting Malpighiaceae and other floral syndromes evolved in parallel across the subtribe, and many clades exhibit extensive variation in pollination-related traits. Because previous classifications heavily emphasized these floral features, many genera recognized were not monophyletic. Our classification based on monophyly will facilitate focused monographs and clarifies the evolution of morphological and biochemical traits of interest within this highly diverse subtribe. © 2011 The Linnean Society of London, Botanical Journal of the Linnean Society, 2012, 168, 117–146.
    Botanical Journal of the Linnean Society 11/2011; 168(2):117 - 146. · 2.70 Impact Factor

Publication Stats

4k Citations
563.79 Total Impact Points

Institutions

  • 1970–2014
    • University of Nevada, Reno
      • Department of Biochemistry and Molecular Biology
      Reno, Nevada, United States
  • 2013
    • University of North Texas
      • Department of Biological Sciences
      Denton, TX, United States
  • 2010
    • Smithsonian Tropical Research Institute
      Ciudad de Panamá, Panamá, Panama
  • 2007
    • Saga University
      • Faculty of Agriculture
      Saga-shi, Saga-ken, Japan
    • Massachusetts General Hospital
      • Department of Molecular Biology
      Boston, MA, United States
  • 1994–2006
    • Oklahoma State University - Stillwater
      • • Department of Biochemistry and Molecular Biology
      • • Department of Plant and Soil Sciences
      Stillwater, Oklahoma, United States
  • 2001
    • Purdue University
      • Center for Plant Environmental Stress Physiology
      West Lafayette, Indiana, United States
  • 1988–1999
    • The University of Arizona
      • • Department of Chemistry and Biochemistry (College of Science)
      • • Department of Molecular and Cellular Biology
      Tucson, AZ, United States
  • 1987–1988
    • Rutgers, The State University of New Jersey
      New Brunswick, New Jersey, United States