Metabolic Adaptation, a Specialized Leaf Organ Structure and Vascular Responses to Diurnal N-2 Fixation by Nostoc azollae Sustain the Astonishing Productivity of Azolla Ferns without Nitrogen Fertilizer

Brouwer P, Bräutigam A, Buijs VA, Tazelaar AOE, van der Werf A, Schlueter U, Reichart G-J, Bolger A, Usadel B, Weber APM, Schluepmann H (2017)
Frontiers in Plant Science 8: 442.

Zeitschriftenaufsatz | Veröffentlicht | Englisch
 
Download
OA 3.65 MB
Autor*in
Brouwer, Paul; Bräutigam, AndreaUniBi ; Buijs, Valerie A.; Tazelaar, Anne O. E.; van der Werf, Adrie; Schlueter, Urte; Reichart, Gert-Jan; Bolger, Anthony; Usadel, Björn; Weber, Andreas P. M.; Schluepmann, Henriette
Abstract / Bemerkung
Sustainable agriculture demands reduced input of man-made nitrogen (N) fertilizer, yet N-2 fixation limits the productivity of crops with heterotrophic diazotrophic bacterial symbionts. We investigated floating ferns from the genus Azolla that host phototrophic diazotrophic Nostoc azollae in leaf pockets and belong to the fastest growing plants. Experimental production reported here demonstrated N-fertilizer independent production of nitrogen-rich biomass with an annual yield potential per ha of 1200 kg(-1) N fixed and 35 t dry biomass. N-15(2) fixation peaked at noon, reaching 0.4 mg N g(-1) dry weight h(-1). Azolla ferns therefore merit consideration as protein crops in spite of the fact that little is known about the fern's physiology to enable domestication. To gain an understanding of their nitrogen physiology, analyses of fern diel transcript profiles under differing nitrogen fertilizer regimes were combined with microscopic observations. Results established that the ferns adapted to the phototrophic N-2-fixing symbionts N. azollae by (1) adjusting metabolically to nightly absence of N supply using responses ancestral to ferns and seed plants; (2) developing a specialized xylem-rich vasculature surrounding the leaf-pocket organ; (3) responding to N-supply by controlling transcripts of genes mediating nutrient transport, allocation and vasculature development. Unlike other non-seed plants, the Azolla fern clock is shown to contain both the morning and evening loops; the evening loop is known to control rhythmic gene expression in the vasculature of seed plants and therefore may have evolved along with the vasculature in the ancestor of ferns and seed plants.
Stichworte
dinitrogen fixation; heterocystous cyanobacteria; aquatic ferns; vasculature; diel cycling; clock evolution; Azolla/Nostoc azollae; symbiosis; RNA-seq
Erscheinungsjahr
2017
Zeitschriftentitel
Frontiers in Plant Science
Band
8
Art.-Nr.
442
ISSN
1664-462X
Page URI
https://pub.uni-bielefeld.de/record/2915122

Zitieren

Brouwer P, Bräutigam A, Buijs VA, et al. Metabolic Adaptation, a Specialized Leaf Organ Structure and Vascular Responses to Diurnal N-2 Fixation by Nostoc azollae Sustain the Astonishing Productivity of Azolla Ferns without Nitrogen Fertilizer. Frontiers in Plant Science. 2017;8: 442.
Brouwer, P., Bräutigam, A., Buijs, V. A., Tazelaar, A. O. E., van der Werf, A., Schlueter, U., Reichart, G. - J., et al. (2017). Metabolic Adaptation, a Specialized Leaf Organ Structure and Vascular Responses to Diurnal N-2 Fixation by Nostoc azollae Sustain the Astonishing Productivity of Azolla Ferns without Nitrogen Fertilizer. Frontiers in Plant Science, 8, 442. doi:10.3389/fpls.2017.00442
Brouwer, Paul, Bräutigam, Andrea, Buijs, Valerie A., Tazelaar, Anne O. E., van der Werf, Adrie, Schlueter, Urte, Reichart, Gert-Jan, et al. 2017. “Metabolic Adaptation, a Specialized Leaf Organ Structure and Vascular Responses to Diurnal N-2 Fixation by Nostoc azollae Sustain the Astonishing Productivity of Azolla Ferns without Nitrogen Fertilizer”. Frontiers in Plant Science 8: 442.
Brouwer, P., Bräutigam, A., Buijs, V. A., Tazelaar, A. O. E., van der Werf, A., Schlueter, U., Reichart, G. - J., Bolger, A., Usadel, B., Weber, A. P. M., et al. (2017). Metabolic Adaptation, a Specialized Leaf Organ Structure and Vascular Responses to Diurnal N-2 Fixation by Nostoc azollae Sustain the Astonishing Productivity of Azolla Ferns without Nitrogen Fertilizer. Frontiers in Plant Science 8:442.
Brouwer, P., et al., 2017. Metabolic Adaptation, a Specialized Leaf Organ Structure and Vascular Responses to Diurnal N-2 Fixation by Nostoc azollae Sustain the Astonishing Productivity of Azolla Ferns without Nitrogen Fertilizer. Frontiers in Plant Science, 8: 442.
P. Brouwer, et al., “Metabolic Adaptation, a Specialized Leaf Organ Structure and Vascular Responses to Diurnal N-2 Fixation by Nostoc azollae Sustain the Astonishing Productivity of Azolla Ferns without Nitrogen Fertilizer”, Frontiers in Plant Science, vol. 8, 2017, : 442.
Brouwer, P., Bräutigam, A., Buijs, V.A., Tazelaar, A.O.E., van der Werf, A., Schlueter, U., Reichart, G.-J., Bolger, A., Usadel, B., Weber, A.P.M., Schluepmann, H.: Metabolic Adaptation, a Specialized Leaf Organ Structure and Vascular Responses to Diurnal N-2 Fixation by Nostoc azollae Sustain the Astonishing Productivity of Azolla Ferns without Nitrogen Fertilizer. Frontiers in Plant Science. 8, : 442 (2017).
Brouwer, Paul, Bräutigam, Andrea, Buijs, Valerie A., Tazelaar, Anne O. E., van der Werf, Adrie, Schlueter, Urte, Reichart, Gert-Jan, Bolger, Anthony, Usadel, Björn, Weber, Andreas P. M., and Schluepmann, Henriette. “Metabolic Adaptation, a Specialized Leaf Organ Structure and Vascular Responses to Diurnal N-2 Fixation by Nostoc azollae Sustain the Astonishing Productivity of Azolla Ferns without Nitrogen Fertilizer”. Frontiers in Plant Science 8 (2017): 442.
Alle Dateien verfügbar unter der/den folgenden Lizenz(en):
Copyright Statement:
Dieses Objekt ist durch das Urheberrecht und/oder verwandte Schutzrechte geschützt. [...]
Volltext(e)
Access Level
OA Open Access
Zuletzt Hochgeladen
2019-09-06T09:18:54Z
MD5 Prüfsumme
63d88ca30f1205b93c8e3486f4b5281f


5 Zitationen in Europe PMC

Daten bereitgestellt von Europe PubMed Central.

Is there foul play in the leaf pocket? The metagenome of floating fern Azolla reveals endophytes that do not fix N2 but may denitrify.
Dijkhuizen LW, Brouwer P, Bolhuis H, Reichart GJ, Koppers N, Huettel B, Bolger AM, Li FW, Cheng S, Liu X, Wong GK, Pryer K, Weber A, Bräutigam A, Schluepmann H., New Phytol 217(1), 2018
PMID: 29084347
Jasmonic and salicylic acid response in the fern Azolla filiculoides and its cyanobiont.
de Vries S, de Vries J, Teschke H, von Dahlen JK, Rose LE, Gould SB., Plant Cell Environ 41(11), 2018
PMID: 29314046
Azolla along a phosphorus gradient: biphasic growth response linked to diazotroph traits and phosphorus-induced iron chlorosis.
Temmink RJM, Harpenslager SF, Smolders AJP, van Dijk G, Peters RCJH, Lamers LPM, van Kempen MML., Sci Rep 8(1), 2018
PMID: 29535346
Growing Azolla to produce sustainable protein feed: the effect of differing species and CO2 concentrations on biomass productivity and chemical composition.
Brouwer P, Schluepmann H, Nierop KG, Elderson J, Bijl PK, van der Meer I, de Visser W, Reichart GJ, Smeekens S, van der Werf A., J Sci Food Agric 98(12), 2018
PMID: 29573358
Fern genomes elucidate land plant evolution and cyanobacterial symbioses.
Li FW, Brouwer P, Carretero-Paulet L, Cheng S, de Vries J, Delaux PM, Eily A, Koppers N, Kuo LY, Li Z, Simenc M, Small I, Wafula E, Angarita S, Barker MS, Bräutigam A, dePamphilis C, Gould S, Hosmani PS, Huang YM, Huettel B, Kato Y, Liu X, Maere S, McDowell R, Mueller LA, Nierop KGJ, Rensing SA, Robison T, Rothfels CJ, Sigel EM, Song Y, Timilsena PR, Van de Peer Y, Wang H, Wilhelmsson PKI, Wolf PG, Xu X, Der JP, Schluepmann H, Wong GK, Pryer KM., Nat Plants 4(7), 2018
PMID: 29967517

80 References

Daten bereitgestellt von Europe PubMed Central.

Relationships for estimating N2 fixation in legumes: incidence for N balance of legume-based cropping systems in Europe.
Anglade, Ecosphere 6(), 2015
Azolla filiculoides as partial replacement for traditional protein supplements in diets for growing-fattening pigs based on sugar cane juice.
Becerra, Livest. Res. Rural Dev. 2(), 1990
Controlling the false discovery rate: a practical and powerful approach to multiple testing.
Benjamini, J. R. Stat. Soc. 57(), 1995
Sugars and circadian regulation make major contributions to the global regulation of diurnal gene expression in Arabidopsis.
Blasing OE, Gibon Y, Gunther M, Hohne M, Morcuende R, Osuna D, Thimm O, Usadel B, Scheible WR, Stitt M., Plant Cell 17(12), 2005
PMID: 16299223
Suppression of Arbuscule Degeneration in Medicago truncatula phosphate transporter4 Mutants is Dependent on the Ammonium Transporter 2 Family Protein AMT2;3.
Breuillin-Sessoms F, Floss DS, Gomez SK, Pumplin N, Ding Y, Levesque-Tremblay V, Noar RD, Daniels DA, Bravo A, Eaglesham JB, Benedito VA, Udvardi MK, Harrison MJ., Plant Cell 27(4), 2015
PMID: 25841038
Azolla domestication towards a biobased economy?
Brouwer P, Brautigam A, Kulahoglu C, Tazelaar AO, Kurz S, Nierop KG, van der Werf A, Weber AP, Schluepmann H., New Phytol. 202(3), 2014
PMID: 24494738
Long-term non-invasive and continuous measurements of legume nodule activity.
Cabeza RA, Liese R, Fischinger SA, Sulieman S, Avenhaus U, Lingner A, Hein H, Koester B, Baumgarten V, Dittert K, Schulze J., Plant J. 81(4), 2015
PMID: 25640854
Are bacteria the third partner of the Azolla-Anabaena symbiosis?
Carrapiço, Plant Soil 137(), 1991
Differential expression of the two Arabidopsis nitrate reductase genes.
Cheng CL, Acedo GN, Dewdney J, Goodman HM, Conkling MA., Plant Physiol. 96(1), 1991
PMID: 16668164
Towards global phosphorus security: a systems framework for phosphorus recovery and reuse options.
Cordell D, Rosemarin A, Schroder JJ, Smit AL., Chemosphere 84(6), 2011
PMID: 21414650
The EU’s dependency on soya bean import for the animal feed industry and potential for EU produced alternatives.
de, OCL 21(), 2014
Cytokinin-induced promotion of root meristem size in the fern Azolla supports a shoot-like origin of euphyllophyte roots.
de Vries J, Fischer AM, Roettger M, Rommel S, Schluepmann H, Brautigam A, Carlsbecker A, Gould SB., New Phytol. 209(2), 2015
PMID: 26358624
Phylogeny.fr: robust phylogenetic analysis for the non-specialist.
Dereeper A, Guignon V, Blanc G, Audic S, Buffet S, Chevenet F, Dufayard JF, Guindon S, Lefort V, Lescot M, Claverie JM, Gascuel O., Nucleic Acids Res. 36(Web Server issue), 2008
PMID: 18424797
Distribution of nitrogen fixation and nitrogenase-like sequences amongst microbial genomes.
Dos Santos PC, Fang Z, Mason SW, Setubal JC, Dixon R., BMC Genomics 13(), 2012
PMID: 22554235
An ultrastructural study of the Azolla, Anabaena azollae relationship.
Duckett, New Phytol. 75(), 1975
Tissue-specific clocks in Arabidopsis show asymmetric coupling.
Endo M, Shimizu H, Nohales MA, Araki T, Kay SA., Nature 515(7527), 2014
PMID: 25363766
How a century of ammonia synthesis changed the world.
Erisman, Nat. Geosci. 1(), 2008
Double trouble: subsidence, and CO2 respiration due to 1,000 years of Dutch coastal peatlands cultivation.
Erkens, Hydrogeol. J. 24(), 2016
Assessing the impact of the green revolution, 1960 to 2000.
Evenson RE, Gollin D., Science 300(5620), 2003
PMID: 12730592
“Effects of antibiotic treatments on Azolla-Anabaena and Arthrobacter,” in
Forni, Nitrogen Fixation (), 1991
Capacities and constraints of amino acid utilization in Arabidopsis.
Forsum O, Svennerstam H, Ganeteg U, Nasholm T., New Phytol. 179(4), 2008
PMID: 18627491
Molecular basis of symbiosis between Rhizobium and legumes.
Freiberg C, Fellay R, Bairoch A, Broughton WJ, Rosenthal A, Perret X., Nature 387(6631), 1997
PMID: 9163424
The oxygen sensitivity of nitrogenase: a problem for biochemists and micro-organisms.
Gallon, Trends Biochem. Sci. 6(), 1981
Nitrogen cycles: past, present, and future.
Galloway JN, Dentener FJ, Capone DG, Boyer EW, Howarth RW, Seitzinger SP, Asner GP, Cleveland CC, Green PA, Holland EA., Biogeochemistry. 70(2), 2004
PMID: IND43744977
Systems approach identifies an organic nitrogen-responsive gene network that is regulated by the master clock control gene CCA1.
Gutierrez RA, Stokes TL, Thum K, Xu X, Obertello M, Katari MS, Tanurdzic M, Dean A, Nero DC, McClung CR, Coruzzi GM., Proc. Natl. Acad. Sci. U.S.A. 105(12), 2008
PMID: 18344319
Crops that feed the World 2. Soybean—worldwide production, use, and constraints caused by pathogens and pests.
Hartman, Food Secur. 3(), 2011
A Preliminary conspectus of the allon flora from the late cretaceous (Late Santonian) of Central Georgia, U.S.A. on JSTOR.
Herendeen, Ann. Mo. Bot. Gard. 86(), 1999
Does the core circadian clock in the moss Physcomitrella patens (Bryophyta) comprise a single loop?
Holm K, Kallman T, Gyllenstrand N, Hedman H, Lagercrantz U., BMC Plant Biol. 10(), 2010
PMID: 20550695
Quantitative analysis of the initial transport of fixed nitrogen in nodulated soybean plants using 15N as a tracer.
Hung, Soil Sci. Plant Nutr. 59(), 2013
The relationship between combined nitrogen uptakes and nitrogen fixation in Azolla-Anabaena symbiosis.
Ito, New Phytolo. 95(), 1983
The Azolla-Anabaena azollae relationship. X. 15N2 fixation and transport in main stem axes.
Kaplan, New Phytol. 89(), 1981
Evolution of signal transduction in intracellular symbiosis.
Kistner C, Parniske M., Trends Plant Sci. 7(11), 2002
PMID: 12417152
Microbiomes of streptophyte algae and bryophytes suggest that a functional suite of microbiota fostered plant colonization of land.
Knack, Int. J. Plant Sci. 176(), 2015
Nutritional value of aquatic ferns (Azolla filiculoides Lam. and Salvinia molesta Mitchell) in pigs
Leterme Pascal, Londono AngelaM, Munoz JaimeE, Suarez Jeimmy, Bedoya CarlosA, Souffrant WolfgangB, Buldgen Andre., Anim. Feed Sci. Technol. 149(1-2), 2009
PMID: IND44159253
Nutritional value and intake of aquatic ferns (Azolla filiculoides Lam. and Salvinia molesta Mitchell.) in sows
Leterme Pascal, Londono AngelaM, Ordonez DianaC, Rosales Alejandra, Estrada Fernando, Bindelle Jerome, Buldgen Andre., Anim. Feed Sci. Technol. 155(1), 2010
PMID: IND44306412
Nostopeptolide plays a governing role during cellular differentiation of the symbiotic cyanobacterium Nostoc punctiforme.
Liaimer A, Helfrich EJ, Hinrichs K, Guljamow A, Ishida K, Hertweck C, Dittmann E., Proc. Natl. Acad. Sci. U.S.A. 112(6), 2015
PMID: 25624477
Carbon dioxide flux from rice paddy soils in central China: effects of intermittent flooding and draining cycles.
Liu Y, Wan KY, Tao Y, Li ZG, Zhang GS, Li SL, Chen F., PLoS ONE 8(2), 2013
PMID: 23437170
Mercator: a fast and simple web server for genome scale functional annotation of plant sequence data.
Lohse M, Nagel A, Herter T, May P, Schroda M, Zrenner R, Tohge T, Fernie AR, Stitt M, Usadel B., Plant Cell Environ. 37(5), 2013
PMID: 24237261
The plant vascular system: evolution, development and functions.
Lucas WJ, Groover A, Lichtenberger R, Furuta K, Yadav SR, Helariutta Y, He XQ, Fukuda H, Kang J, Brady SM, Patrick JW, Sperry J, Yoshida A, Lopez-Millan AF, Grusak MA, Kachroo P., J Integr Plant Biol 55(4), 2013
PMID: 23462277
Nitrite transport activity of a novel HPP family protein conserved in cyanobacteria and chloroplasts.
Maeda S, Konishi M, Yanagisawa S, Omata T., Plant Cell Physiol. 55(7), 2014
PMID: 24904028
Evolution of Electrogenic Ammonium Transporters (AMTs).
McDonald TR, Ward JM., Front Plant Sci 7(), 2016
PMID: 27066024
Physiological adaptations in nitrogen fixing Nostoc-plant symbiotic associations.
Meeks, Microbiol. Monogr. 8(), 2009
Azolla-Anabaena Relationship : XIII. Fixation of [N]N(2).
Meeks JC, Steinberg NA, Enderlin CS, Joseph CM, Peters GA., Plant Physiol. 84(3), 1987
PMID: 16665538
Phylogeny and divergence time estimates for the fern genus Azolla (Salviniaceae).
Metzgar JS, Schneider H, Pryer KM., Int. J. Plant Sci. 168(7), 2007
PMID: IND43960855
Molecular mechanisms underlying the Arabidopsis circadian clock.
Nakamichi N., Plant Cell Physiol. 52(10), 2011
PMID: 21873329
Channel-like NH3 flux by ammonium transporter AtAMT2.
Neuhauser B, Dynowski M, Ludewig U., FEBS Lett. 583(17), 2009
PMID: 19635480
Comparing the potential production and value of high-energy liquid fuels and protein from marine and freshwater macroalgae.
Neveux, Global Change Biol. Bioenergy 7(), 2015
Clocks in algae.
Noordally ZB, Millar AJ., Biochemistry 54(2), 2014
PMID: 25379817
Effect of ammonia on nitrogen fixation by the blue-green alga Anabaena cylindrica.
Ohmori, Plant Cell Physiol. 15(), 1974
Biotechnological solutions to the nitrogen problem.
Oldroyd GE, Dixon R., Curr. Opin. Biotechnol. 26(), 2013
PMID: 24679253
Robust biological nitrogen fixation in a model grass-bacterial association.
Pankievicz VC, do Amaral FP, Santos KF, Agtuca B, Xu Y, Schueller MJ, Arisi AC, Steffens MB, de Souza EM, Pedrosa FO, Stacey G, Ferrieri RA., Plant J. 81(6), 2015
PMID: 25645593
The Azolla-Anabaena symbiosis - basic biology.
Peters, Annu. Rev. Plant Physiol. Plant Mol. Biol. 40(), 1989
Characterization and comparison of five N2-fixing Azolla-Anabaena associations, I. Optimization of growth conditions for biomass increase and N content in a controlled environment.
Peters, Plant Cell Environ. 3(), 1980
Tansley review no. 116: Cyanobacterium-plant symbioses.
Rai AN, Soderback E, Bergman B., New Phytol. 147(3), 2000
PMID: IND22079133
Algae-bacteria interactions: Evolution, ecology and emerging applications.
Ramanan R, Kim BH, Cho DH, Oh HM, Kim HS., Biotechnol. Adv. 34(1), 2015
PMID: 26657897
Genome erosion in a nitrogen-fixing vertically transmitted endosymbiotic multicellular cyanobacterium.
Ran L, Larsson J, Vigil-Stenman T, Nylander JA, Ininbergs K, Zheng WW, Lapidus A, Lowry S, Haselkorn R, Bergman B., PLoS ONE 5(7), 2010
PMID: 20628610
edgeR: a Bioconductor package for differential expression analysis of digital gene expression data.
Robinson MD, McCarthy DJ, Smyth GK., Bioinformatics 26(1), 2009
PMID: 19910308
Genome-wide reprogramming of primary and secondary metabolism, protein synthesis, cellular growth processes, and the regulatory infrastructure of Arabidopsis in response to nitrogen.
Scheible WR, Morcuende R, Czechowski T, Fritz C, Osuna D, Palacios-Rojas N, Schindelasch D, Thimm O, Udvardi MK, Stitt M., Plant Physiol. 136(1), 2004
PMID: 15375205
The Azolla-Anabaena association: historical perspective, symbiosis and energy metabolism.
Shi, Bot. Rev. 54(), 1988
Plant based phosphorus recovery from wastewater via algae and macrophytes.
Shilton AN, Powell N, Guieysse B., Curr. Opin. Biotechnol. 23(6), 2012
PMID: 22889679
MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes.
Thimm O, Blasing O, Gibon Y, Nagel A, Meyer S, Kruger P, Selbig J, Muller LA, Rhee SY, Stitt M., Plant J. 37(6), 2004
PMID: 14996223
High-resolution whole-mount imaging of three-dimensional tissue organization and gene expression enables the study of Phloem development and structure in Arabidopsis.
Truernit E, Bauby H, Dubreucq B, Grandjean O, Runions J, Barthelemy J, Palauqui JC., Plant Cell 20(6), 2008
PMID: 18523061
Transport and metabolism in legume-rhizobia symbioses.
Udvardi M, Poole PS., Annu Rev Plant Biol 64(), 2013
PMID: 23451778
The pore of the leaf cavity of Azolla: morphology, cytochemistry and possible functions.
Veys, Symbiosis 27(), 1999
Integrated RNA-seq and sRNA-seq analysis identifies novel nitrate-responsive genes in Arabidopsis thaliana roots.
Vidal EA, Moyano TC, Krouk G, Katari MS, Tanurdzic M, McCombie WR, Coruzzi GM, Gutierrez RA., BMC Genomics 14(), 2013
PMID: 24119003
Azolla: a review of its biology and utilization.
Wagner, Bot. Rev. 63(), 1997

Watanabe, Biofertilizer Germplasm Collections at IRRI. (), 1992
Genetic Gain × Management Interactions in Soybean: II. Nitrogen Utilization.
Wilson, Crop Sci. 54(340), 2014
Plant nitrogen assimilation and use efficiency.
Xu G, Fan X, Miller AJ., Annu Rev Plant Biol 63(), 2012
PMID: 22224450
Systemic and local effects of long-term application of nitrate on nodule growth and N2 fixation in soybean (Glycine max [L.] Merr.).
Yashima, Soil Sci. Plant Nutr. 49(), 2003
Export

Markieren/ Markierung löschen
Markierte Publikationen

Open Data PUB

Web of Science

Dieser Datensatz im Web of Science®
Quellen

PMID: 28408911
PubMed | Europe PMC

Suchen in

Google Scholar