Get 20M+ Full-Text Papers For Less Than $1.50/day. Start a 14-Day Trial for You or Your Team.

Learn More →

Molecular level responses to chronic versus pulse nutrient loading in the seagrass Posidonia oceanica undergoing herbivore pressure

Molecular level responses to chronic versus pulse nutrient loading in the seagrass Posidonia... Seagrasses are key marine foundation species, currently declining due to the compounded action of global and regional anthropogenic stressors. Eutrophication has been associated with seagrass decline, while grazing has been traditionally considered to be a natural disturbance with a relatively low impact on seagrasses. In the recent years, this assumption has been revisited. Here, by means of a 16-month field-experiment, we investigated the molecular mechanisms driving the long-term response of Posidonia oceanica to the combination of nutrient enrichment, either as a chronic (press) or pulse disturbance, and herbivory. Changes in expression levels of 19 target genes involved in key steps of photosynthesis, nutrient assimilation, chlorophyll metabolism, oxidative-stress response and plant defense were evaluated through reverse transcription–quantitative polymerase chain reaction (RT-qPCR). High herbivore pressure affected the molecular response of P. oceanica more dramatically than did enhanced nutrient levels, altering the expression of genes involved in plant tolerance and resistance traits, such as photosynthesis and defense mechanisms. Genes involved in carbon fixation and N assimilation modulated the response of plants to high nutrient levels. Availability of resources seems to modify P. oceanica response to herbivory, where the upregulation of a nitrate transporter gene was accompanied by the decline in the expression of nitrate reductase in the leaves, suggesting a change in plant-nutrient allocation strategy. Finally, press and pulse fertilizations altered nitrate uptake and reduction-related genes in opposite ways, suggesting that taking into account the temporal regime of nutrient loading is important to assess the physiological response of seagrasses to eutrophication. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Oecologia Springer Journals

Molecular level responses to chronic versus pulse nutrient loading in the seagrass Posidonia oceanica undergoing herbivore pressure

Download PDF
17 pages

Loading next page...
 
/lp/springer_journal/molecular-level-responses-to-chronic-versus-pulse-nutrient-loading-in-VuDy5V33TX
Publisher
Springer Journals
Copyright
Copyright © 2018 by Springer-Verlag GmbH Germany, part of Springer Nature
Subject
Life Sciences; Ecology; Plant Sciences; Hydrology/Water Resources
ISSN
0029-8549
eISSN
1432-1939
DOI
10.1007/s00442-018-4172-9
Publisher site
See Article on Publisher Site

Abstract

Seagrasses are key marine foundation species, currently declining due to the compounded action of global and regional anthropogenic stressors. Eutrophication has been associated with seagrass decline, while grazing has been traditionally considered to be a natural disturbance with a relatively low impact on seagrasses. In the recent years, this assumption has been revisited. Here, by means of a 16-month field-experiment, we investigated the molecular mechanisms driving the long-term response of Posidonia oceanica to the combination of nutrient enrichment, either as a chronic (press) or pulse disturbance, and herbivory. Changes in expression levels of 19 target genes involved in key steps of photosynthesis, nutrient assimilation, chlorophyll metabolism, oxidative-stress response and plant defense were evaluated through reverse transcription–quantitative polymerase chain reaction (RT-qPCR). High herbivore pressure affected the molecular response of P. oceanica more dramatically than did enhanced nutrient levels, altering the expression of genes involved in plant tolerance and resistance traits, such as photosynthesis and defense mechanisms. Genes involved in carbon fixation and N assimilation modulated the response of plants to high nutrient levels. Availability of resources seems to modify P. oceanica response to herbivory, where the upregulation of a nitrate transporter gene was accompanied by the decline in the expression of nitrate reductase in the leaves, suggesting a change in plant-nutrient allocation strategy. Finally, press and pulse fertilizations altered nitrate uptake and reduction-related genes in opposite ways, suggesting that taking into account the temporal regime of nutrient loading is important to assess the physiological response of seagrasses to eutrophication.

Journal

Oecologia – Springer Journals

Published: May 29, 2018

References

  • Shoot growth and nitrogen responses to simulated herbivory in Kenyan seagrasses
    Alcoverro, T; Mariani, S
  • Differential activity of peroxidase isozymes in response to wounding, gypsy moth, and plant hormones in northern red oak (Quercus rubra L.)
    Allison, SD; Schultz, JC
  • Normalization of real-time quantitative reverse transcription-PCR data: a model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets
    Andersen, CL; Jensen, JL; Ørntoft, TF
  • Wound-induced accumulations of condensed tannins in turtlegrass, Thalassia testudinum
    Arnold, TM; Tanner, CE; Rothen, M; Bullington, J
  • Effects of enhanced loads of nutrients on epiphytes on leaves and rhizomes of Posidonia oceanica
    Balata, D; Piazzi, L; Nesti, U; Bulleri, F; Bertocci, I
  • The importance of the variance around the mean effect size of ecological processes
    Benedetti-Cecchi, L
  • Population-specificity of heat stress gene induction in northern and southern eelgrass Zostera marina populations under simulated global warming
    Bergmann, N; Winters, G; Gauch, G; Eizaguirre, C; Gu, J; Nelle, P; Fricke, B; Reusch, TBH
  • Defensive role of tomato polyphenol oxidases against cotton bollworm (Helicoverpa armigera) and beet armyworm (Spodoptera exigua)
    Bhonwong, A; Stout, MJ; Attajarusit, J; Tantasawat, P
  • Epigenetics for ecologists
    Bossdorf, O; Richards, CL; Pigliucci, M
  • Is photosynthetic transcriptional regulation in Triticum aestivum L. cv. ‘TugelaDN’a contributing factor for tolerance to Diuraphis noxia (Homoptera: Aphididae)?
    Botha, A-M; Lacock, L; Niekerk, C; Matsioloko, MT; Preez, FB; Loots, S; Venter, E; Kunert, KJ; Cullis, CA
  • Herbivore vs. nutrient control of marine primary producers: context-dependent effects
    Burkepile, DE; Hay, ME
  • Seagrasses and eutrophication
    Burkholder, JM; Tomasko, DA; Touchette, BW
  • Seagrass collapse due to synergistic stressors is not anticipated by phenological changes
    Ceccherelli, G; Oliva, S; Pinna, S; Piazzi, L; Procaccini, G; Marín-Guirao, L; Dattolo, E; Gallia, R; Manna, G; Gennaro, P; Costa, MM; Barrote, I; Silva, J; Bulleri, F
  • Marine megaherbivore grazing may increase seagrass tolerance to high nutrient loads
    Christianen, MJA; Govers, LL; Bouma, TJ; Kiswara, W; Roelofs, JGM; Lamers, LPM; Katwijk, MM
  • Habitat collapse due to overgrazing threatens turtle conservation in marine protected areas
    Christianen, MJA; Herman, PMJ; Bouma, TJ; Lamers, LPM; Katwijk, MM; Heide, T; Mumby, PJ; Silliman, BR; Engelhard, SL; Kerk, M; Kiswara, W; Koppel, J
  • PRIMER v6: user manual/tutorial
    Clarke, K; Gorley, R
  • The value of the world’s ecosystem services and natural capital
    Costanza, R; d’Arge, R; Groot, R; Farber, S; Grasso, M; Hannon, B; Limburg, K; Naeem, S; O’Neill, RV; Paruelo, J; Raskin, RG; Sutton, P; Belt, M
  • Transcriptome characterisation and simple sequence repeat marker discovery in the seagrass Posidonia oceanica
    D’Esposito, D; Orrù, L; Dattolo, E; Bernardo, L; Lamontanara, A; Orsini, L; Serra, I; Mazzuca, S; Procaccini, G
  • Response of the seagrass Posidonia oceanica to different light environments: insights from a combined molecular and photo-physiological study
    Dattolo, E; Ruocco, M; Brunet, C; Lorenti, M; Lauritano, C; D’Esposito, D; Luca, P; Sanges, R; Mazzuca, S; Procaccini, G
  • Adjusting to global change through clonal growth and epigenetic variation
    Dodd, RS; Douhovnikoff, V
  • Seagrass nutrient content
    Duarte, CM
  • Submerged aquatic vegetation in relation to different nutrient regimes
    Duarte, CM
  • The future of seagrass meadows
    Duarte, CM
  • The importance of grazing intensity and frequency for physiological responses of the tropical seagrass Thalassia hemprichii
    Eklöf, JS; Gullström, M; Björk, M; Asplund, ME; Hammar, L; Dahlgren, A; Öhman, MC
  • Effects of excluding sea turtle herbivores from a seagrass bed: overgrazing may have led to loss of seagrass meadows in Bermuda
    Fourqurean, JW; Manuel, S; Coates, KA; Kenworthy, WJ; Smith, SR
  • Transcriptomic resilience to global warming in the seagrass Zostera marina, a marine foundation species
    Franssen, SU; Gu, J; Bergmann, N; Winters, G; Klostermeier, UC; Rosenstiel, P; Bornberg-Bauer, E; Reusch, TBH
  • Herbivore-induced shifts in carbon and nitrogen allocation in red oak seedlings
    Frost, CJ; Hunter, MD
  • Structure and function of plant-type ferredoxins
    Fukuyama, K
  • Methods of seawater analysis
  • Multiple stressors in a changing world: the need for an improved perspective on physiological responses to the dynamic marine environment
    Gunderson, AR; Armstrong, EJ; Stillman, JH
  • Gene expression profiling of tolerant barley in response to Diuraphis noxia (Hemiptera: Aphididae) feeding
    Gutsche, A; Heng-Moss, T; Sarath, G; Twigg, P; Xia, Y; Lu, G; Mornhinweg, D
  • PAST: paleontological statistics software package for education and data analysis
    Hammer, Ø; Harper, D; Ryan, P
  • Eelgrass Zostera marina loss in temperate estuaries: relationship to land-derived nitrogen loads and effect of light limitation imposed by algae
    Hauxwell, J; Cebrián, J; Valiela, I
  • Effects of nutrient enrichment and grazing on shoalgrass Halodule wrightii and its epiphytes: results of a field experiment
    Heck, KL; Valentine, JF; Pennock, JR; Chaplin, G; Spitzer, PM
  • Seagrass genotypic diversity increases disturbance response via complementarity and dominance
    Hughes, AR; Stachowicz, JJ
  • Relative effects of grazers and nutrients on seagrasses: a meta-analysis approach
    Hughes, AR; Bando, KJ; Rodriguez, LF; Williams, SL
  • Effects of nitrogen addition on nitrogen metabolism and carbon reserves in the temperate seagrass Posidonia oceanica
    Invers, O; Kraemer, GP; Pérez, M; Romero, J
  • Grazing history, defoliation, and competition: effects on shortgrass production and nitrogen accumulation
    Jaramillo, VJ; Detling, JK
  • Diagnostic gene expression biomarkers of coral thermal stress
    Kenkel, CD; Sheridan, C; Leal, MC; Bhagooli, R; Castillo, KD; Kurata, N; Mcginty, E; Goulet, TL; Matz, MV
  • Plant responses to insect herbivory: interactions between photosynthesis, reactive oxygen species and hormonal signalling pathways
    Kerchev, PI; Fenton, B; Foyer, CH; Hancock, RD
  • Parrotfish grazing on turtlegrass Thalassia testudinum: evidence for the importance of seagrass consumption in food web dynamics of the Florida Keys National Marine Sanctuary
    Kirsch, KD; Valentine, JF; Heck, KL
  • Response of key stress-related genes of the seagrass Posidonia oceanica in the vicinity of submarine volcanic vents
    Lauritano, C; Ruocco, M; Dattolo, E; Buia, MC; Silva, J; Santos, R; Olivé, I; Costa, MM; Procaccini, G
  • Gene expression profiling: opening the black box of plant ecosystem responses to global change
    Leakey, AD; Ainsworth, EA; Bernard, SM; Markelz, RJ; Ort, DR; Placella, SA; Rogers, A; Smith, MD; Sudderth, EA; Weston, DJ; Wullschleger, SD; Yuan, S
  • Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method
    Livak, KJ; Schmittgen, TD
  • A unified approach to marine plant-herbivore interactions. I. populations and communities
    Lubchenco, J; Gaines, SD
  • Molecular indicators of chronic seagrass stress: a new era in the management of seagrass ecosystems?
    Macreadie, PI; Schliep, MT; Rasheed, MA; Chartrand, KM; Ralph, PJ
  • Molecular mechanisms behind the physiological resistance to intense transient warming in an iconic marine plant
    Marín-Guirao, L; Entrambasaguas, L; Dattolo, E; Ruiz, JM; Procaccini, G
  • Specificity in mesograzer-induced defences in seagrasses
    Martínez-Crego, B; Arteaga, P; Ueber, A; Engelen, AH; Santos, R; Molis, M
  • Establishing research strategies, methodologies and technologies to link genomics and proteomics to seagrass productivity, community metabolism, and ecosystem carbon fluxes
    Mazzuca, S; Bjork, M; Beer, S; Felisberto, P; Gobert, S; Procaccini, G; Runcie, J; Silva, J; Borges, AV; Brunet, C; Buapet, P; Champenois, W; Costa, MM; D’Esposito, D; Gullstrom, M; Lejeune, P; Lepoint, G; Olive, I; Rasmusson, LM; Richir, J; Ruocco, M; Serra, IA; Spadafora, A; Santos, R
  • Compensation of nutrient pollution by herbivores in seagrass meadows
    McSkimming, C; Tanner, JE; Russell, BD; Connell, SD
  • Nitrogen storage and remobilization by trees: ecophysiological relevance in a changing world
    Millard, P; Grelet, GA
  • Interactions among temporal patterns determine the effects of multiple stressors
    Molinos, JG; Donohue, I
  • Simulated green turtle grazing affects structure and productivity of seagrass pastures
    Moran, KL; Bjorndal, KA
  • Nutrient presses and pulses differentially impact plants, herbivores, detritivores and their natural enemies
    Murphy, SM; Wimp, GM; Lewis, D; Denno, RF
  • Is PsbS the site of non-photochemical quenching in photosynthesis?
    Niyogi, KK; Li, XP; Rosenberg, V; Jung, HS
  • The evolution of resistance and tolerance to herbivores
    Núñez-Farfán, J; Fornoni, J; Valverde, PL
  • Nitrate transport, sensing, and responses in plants
    O’Brien, JA; Vega, A; Bouguyon, E; Krouk, G; Gojon, A; Coruzzi, G; Gutiérrez Rodrigo, A
  • Characterization of a two-component high-affinity nitrate uptake system in Arabidopsis. Physiology and protein–protein interaction
    Orsel, M; Chopin, F; Leleu, O; Smith, SJ; Krapp, A; Daniel-Vedele, F; Miller, AJ
  • Top-down control as important as nutrient enrichment for eutrophication effects in North Atlantic coastal ecosystems
    Östman, Ö; Eklöf, J; Eriksson, BK; Olsson, J; Moksnes, PO; Bergström, U
  • Molecular physiology reveals ammonium uptake and related gene expression in the seagrass Zostera muelleri
    Pernice, M; Sinutok, S; Sablok, G; Commault, AS; Schliep, M; Macreadie, PI; Rasheed, MA; Ralph, PJ
  • Determination of stable housekeeping genes, differentially regulated target genes and sample integrity: BestKeeper—excel-based tool using pair-wise correlations
    Pfaffl, M; Tichopad, A; Prgomet, C; Neuvians, T
  • Fish herbivory leads to shifts in seagrass Posidonia oceanica investments in sexual reproduction
    Planes, S; Raventos, N; Ferrari, B; Alcoverro, T
  • Extensive direct measurements of Posidonia oceanica defoliation confirm the importance of herbivory in temperate seagrass meadows
    Prado, P; Tomas, F; Alcoverro, T; Romero, J
  • Nutrient status, plant availability and seasonal forcing mediate fish herbivory in temperate seagrass beds
    Prado, P; Romero, J; Alcoverro, T
  • Depth-specific fluctuations of gene expression and protein abundance modulate the photophysiology in the seagrass Posidonia oceanica
    Procaccini, G; Ruocco, M; Marín-Guirao, L; Dattolo, E; Brunet, C; D’Esposito, D; Lauritano, C; Mazzuca, S; Serra, IA; Bernardo, L; Piro, A; Beer, S; Björk, M; Gullström, M; Buapet, P; Rasmusson, LM; Felisberto, P; Gobert, S; Runcie, JW; Silva, J; Olivé, I; Costa, MM; Barrote, I; Santos, R
  • Nutrient loading fosters seagrass productivity under ocean acidification
    Ravaglioli, C; Lauritano, C; Buia, MC; Balestri, E; Capocchi, A; Fontanini, D; Pardi, G; Tamburello, L; Procaccini, G; Bulleri, F
  • Macro-grazer herbivory regulates seagrass response to pulse and press nutrient loading
    Ravaglioli, C; Capocchi, A; Fontanini, D; Mori, G; Nuccio, C; Bulleri, F
  • Nitrate reductase activity in Zostera marina
    Roth, NC; Pregnall, AM
  • Genome-wide transcriptional reprogramming in the seagrass Cymodocea nodosa under experimental ocean acidification
    Ruocco, M; Musacchia, F; Olivé, I; Costa, MM; Barrote, I; Santos, R; Sanges, R; Procaccini, G; Silva, J
  • Synergistic effects of altered salinity and temperature on estuarine eelgrass (Zostera marina) seedlings and clonal shoots
    Salo, T; Pedersen, MF
  • Herbivores
    Sánchez-Sánchez, H; Morquecho-Contreras, A
  • Tolerance responses to simulated herbivory in the seagrass Cymodocea nodosa
    Sanmartí, N; Saiz, L; Llagostera, I; Pérez, M; Romero, J
  • Flexible resource allocation during plant defense responses
    Schultz, JC; Appel, HM; Ferrieri, AP; Arnold, TM
  • Why does herbivore attack reconfigure primary metabolism?
    Schwachtje, J; Baldwin, IT
  • Reference genes assessment for the seagrass Posidonia oceanica in different salinity, pH and light conditions
    Serra, IA; Lauritano, C; Dattolo, E; Puoti, A; Nicastro, S; Innocenti, AM; Procaccini, G
  • Natural and human-induced disturbance of seagrasses
    Short, FT; Wyllie-Echeverria, S
  • The evolutionary ecology of tolerance to consumer damage
    Stowe, KA; Marquis, RJ; Hochwender, CG; Simms, EL
  • The ecology and evolution of plant tolerance to herbivory
    Strauss, SY; Agrawal, AA
  • Compensation for herbivory by Cucumis sativus through increased photosynthetic capacity and efficiency
    Thomson, VP; Cunningham, SA; Ball, MC; Nicotra, AB
  • Mechanisms of tolerance to herbivore damage: what do we know?
    Tiffin, P
  • Seasonal and small-scale spatial variability of herbivory pressure on the temperate seagrass Posidonia oceanica
    Tomas, F; Turon, X; Romero, J
  • Overview of the physiological ecology of carbon metabolism in seagrasses
    Touchette, BW; Burkholder, JM
  • Review of nitrogen and phosphorus metabolism in seagrasses
    Touchette, BW; Burkholder, JM
  • Plant compensation for arthropod herbivory
    Trumble, J; Kolodny-Hirsch, D; Ting, I
  • Effect of chronic versus pulse perturbations on a marine ecosystem: integration of functional responses across organization levels
    Tuya, F; Betancor, S; Viera-Rodríguez, MA; Guedes, R; Riera, R; Haroun, R; Espino, F
  • Primer3—new capabilities and interfaces
    Untergasser, A; Cutcutache, I; Koressaar, T; Ye, J; Faircloth, BC; Remm, M; Rozen, SG
  • Biochemical and enzymatic changes in rice plants as a mechanism of defense
    Usha Rani, P; Jyothsna, Y
  • The central role of grazing in seagrass ecology. Seagrasses: biology, ecology and conservation
    Valentine, JF; Duffy, JE
  • Experimental evidence that herbivory increases shoot density and productivity in a subtropical turtlegrass (Thalassia testudinum) meadow
    Valentine, JF; Heck, KL; Busby, J; Webb, D
  • Effects of simulated herbivory on nitrogen enzyme levels, assimilation and allocation in Thalassia testudinum
    Valentine, JF; Blythe, EF; Madhavan, S; Sherman, TD
  • Ammonium toxicity in eelgrass Zostera marina
    Katwijk, M; Vergeer, L; Schmitz, G; Roelofs, J
  • Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes
    Vandesompele, J; Preter, K; Pattyn, F; Poppe, B; Roy, N; Paepe, A; Speleman, F
  • Experimental evidence of chemical deterrence against multiple herbivores in the seagrass Posidonia oceanica
    Verges, A; Becerro, MA; Alcoverro, T; Romero, J
  • Compensation and resistance to herbivory in seagrasses: induced responses to simulated consumption by fish
    Verges, A; Perez, M; Alcoverro, T; Romero, J
  • Elevated ammonium concentrations and low light form a dangerous synergy for eelgrass Zostera marina
    Villazán, B; Pedersen, MF; Brun, FG; Vergara, JJ
  • High ammonium availability amplifies the adverse effect of low salinity on eelgrass Zostera marina
    Villazán, B; Salo, T; Brun, FG; Vergara, JJ; Pedersen, MF
  • Uptake, allocation and signaling of nitrate
    Wang, YY; Hsu, PK; Tsay, YF
  • Mechanisms of plant defense against insect herbivores
    War, AR; Paulraj, MG; Ahmad, T; Buhroo, AA; Hussain, B; Ignacimuthu, S; Sharma, HC
  • Physiological and morphological responses of the temperate seagrass Zostera muelleri to multiple stressors: investigating the interactive effects of light and temperature
    York, PH; Gruber, RK; Hill, R; Ralph, PJ; Booth, DJ; Macreadie, PI
  • Induction of the activities of antioxidative enzymes and the levels of malondialdehyde in cucumber seedlings as a consequence of Bemisia tabaci (Hemiptera: Aleyrodidae) infestation
    Zhang, SZ; Hua, BZ; Zhang, F
  • Alteration of plant primary metabolism in response to insect herbivory
    Zhou, S; Lou, YR; Tzin, V; Jander, G