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Journal of Plant Growth Regulation

, Volume 32, Issue 1, pp 31–52 | Cite as

Brassica napus Growth is Promoted by Ascophyllum nodosum (L.) Le Jol. Seaweed Extract: Microarray Analysis and Physiological Characterization of N, C, and S Metabolisms

  • Laëtitia Jannin
  • Mustapha Arkoun
  • Philippe Etienne
  • Philippe Laîné
  • Didier Goux
  • Maria Garnica
  • Marta Fuentes
  • Sara San Francisco
  • Roberto Baigorri
  • Florence Cruz
  • Fabrice Houdusse
  • José-Maria Garcia-Mina
  • Jean-Claude Yvin
  • Alain OurryEmail author
Article

Abstract

Despite its high capacity to take up nitrate from soil, winter rapeseed (Brassica napus) is characterized by a low N recovery in seeds. Thus, to maintain yield, rapeseed requires a high fertilization rate. Increasing nutrient use efficiency in rapeseed by addition of a biostimulant could help improve its agroenvironmental balance. The effects of marine brown seaweed Ascophyllum nodosum on plant growth have been well described physiologically. However, to our knowledge, no study has focused on transcriptomic analyses to determine metabolic targets of these extracts. A preliminary screening of different extracts revealed a significant effect of one of them (AZAL5) on rapeseed root (+102 %) and shoot (+23 %) growth. Microarray analysis was then used on AZAL5-treated or nontreated plants to characterize changes in gene expression that were further supported by physiological evidence. Stimulation of nitrogen uptake (+21 and +115 % in shoots and roots, respectively) and assimilation was increased in a similar manner to growth, whereas sulfate content (+63 and +133 % in shoots and roots, respectively) was more strongly stimulated leading to sulfate accumulation. Among the identified genes whose expression was affected by AZAL5, MinE, a plastid division regulator, was the most strongly affected. Its effect was supported by microscopic analysis showing an enhancement of chloroplast number per cell and starch content but without a significant difference in net photosynthetic rate. In conclusion, it is suggested that AZAL5, which promotes plant growth and nutrient uptake, could be used as a supplementary tool to improve rapeseed agroenvironmental balance.

Keywords

Brassica napus Seaweed extract Ascophyllum nodosum Microarray analysis Growth promotion Nutrient uptake Chloroplast 

Notes

Acknowledgments

This study was part of the AZOSTIMER project, selected and supported by the Pôle de compétitivité Mer-Bretagne, and funded by French FUI (Fond Unique Interministériel), Brittany Region and Saint-Malo Agglomeration. The authors thank Marie-Paule Bataillé and Raphaël Ségura for IRMS analyses and Angel-Mari Zamarreño for analyses of phytohormones. The authors acknowledge Patrick Beauclair for LICOR measurement, Julie Levallois for technical assistance in RNA extractions and q-PCR analyses, Xavier Sarda and Anne-Françoise Ameline for helping with plant culture and harvest, and finally Nicolas Elie from GRECAN (Groupe Régional d’Etude sur le CANcer, Histo-imagerie quantitative, Caen, France) for microscopy image analyses. The authors thank Laurence Cantrill for improving the English of the manuscript.

Supplementary material

344_2012_9273_MOESM1_ESM.doc (1.9 mb)
Supplementary Table 1 List of the differentially expressed genes in shoots and roots of rapeseed after 3 days of AZAL5 supply to the roots (DOC 1923 kb)
344_2012_9273_MOESM2_ESM.doc (1.9 mb)
Supplementary Table 2 List of the differentially expressed genes in shoots and roots of rapeseed after 30 days of AZAL5 supply to the roots (DOC 1981 kb)

References

  1. Abdallah M, Etienne P, Ourry A, Meuriot F (2011) Do initial S reserve and mineral S availability alter leaf S–N mobilization and leaf senescence in oilseed rape? Plant Sci 180:511–520PubMedCrossRefGoogle Scholar
  2. Agostini F, Tei F, Silgram M, Farnselli M, Benincasa P, Aller MF (2010) Decreasing nitrate leaching in vegetable crops with better N management. Genet Eng Biofertil Soil QualOrgan Farm Sustain Agric Rev 4:147–200CrossRefGoogle Scholar
  3. Aguirre E, Leménager D, Bacaicoa E, Fuentes M, Baigorri R, Zamarreño AM, García-Mina JM (2009) The root application of a purified leonardite humic acid modifies the transcriptional regulation of the main physiological root responses to Fe deficiency in Fe-sufficient cucumber plants. Plant Physiol Biochem 47:215–223PubMedCrossRefGoogle Scholar
  4. Blunden G, Gordon SM (1986) Betaines and their sulphono analogues in marine algae. In: Round FE, Chapman DJ (eds) Progress in phycological research, vol 4. Biopress Ltd, Bristol, pp 39–80Google Scholar
  5. Borda T, Celi L, Zavattaro L, Sacco D, Barberis E (2011) Effect of agronomic management on risk of suspended solids and phosphorus losses from soil to water. J. Soil Sediment 11:440–451CrossRefGoogle Scholar
  6. Briand X (1998) IPA-systemic nutrition in foliar fertilisers. Agro Food Ind Hi Tech 9:5–10Google Scholar
  7. Bungard R, Wingler A, Morton J, Andrews M, Press M, Scholes J (1999) Ammonium can stimulate nitrate and nitrite reductase in the absence of nitrate in Clematis vitalba. Plant Cell Environ 22:859–866CrossRefGoogle Scholar
  8. Cardon ZG, Berry J (1992) Effects of O2 and CO2 concentration on the steady-state fluorescence yield of single guard cell pairs of intact leaf discs of Tradescantia albiflora: evidence for Rubisco-mediated carbon fixation and photorespiration in guard cells. Plant Physiol 99:1238–1244PubMedCrossRefGoogle Scholar
  9. Castaings L, Marchive C, Meyer C, Krapp A (2011) Nitrogen signaling in Arabidopsis thaliana: how to obtain insights into a complex signaling network. J Exp Bot 62:1391–1397PubMedCrossRefGoogle Scholar
  10. Cluzet S, Terregrosa C, Jacquet C, Lafitte C, Fournier J, Mercier L, Salamagne S, Briand X, Esquerré-Tugayé MT, Dumas B (2004) Gene expression profiling and protection of Medicago truncatula against a fungal infection in response to an elicitor from green algae Ulva ssp. Plant Cell Environ 27:917–928Google Scholar
  11. Collier MD, Fotelli MN, Kopriva S, Rennenberg H, Hanke DE, Geßler A (2003) Regulation of nitrogen uptake by Fagus sylvatica on a whole plant level—interactions between cytokinins and soluble N compounds. Plant Cell Environ 26:1549–1560CrossRefGoogle Scholar
  12. Craigie JS (2011) Seaweed extract stimuli in plant science and agriculture. J Appl Phycol 23:371–393CrossRefGoogle Scholar
  13. Crouch IJ, Van Staden J (1992) Effect of seaweed concentrate on the establishment and yield of greenhouse tomato plants. J Appl Phycol 4:291–296CrossRefGoogle Scholar
  14. Daniel-Vedele F, Filleur S, Caboche M (1998) Nitrate transport: a key step in nitrate assimilation. Curr Opin Plant Biol 1:235–239PubMedCrossRefGoogle Scholar
  15. Dejoux JF, Recous S, Meynard JM, Trinsoutrot I, Leterme P (2000) The fate of nitrogen from winter-frozen rapeseed leaves: mineralization, fluxes to the environment and uptake by rapeseed crop in spring. Plant Soil 218:257–272CrossRefGoogle Scholar
  16. Desclos M, Dubousset L, Etienne P, Bonnefoy J, Lecahérec F, Satoh H, Ourry A, Avice JC (2008) A proteomic profiling approach to reveal a novel role of BnD22 (Brassica napus drought 22)/ water soluble chlorophyll binding protein in young leaves during nitrogen remobilization induced by stressful condition. Plant Physiol 147:1830–1844PubMedCrossRefGoogle Scholar
  17. Dreccer MF, Schapendonk AHM, Slafer GA, Rabbinge R (2000) Comparative response of wheat and oilseed rape to nitrogen supply: absorption and utilization efficiency of radiation and nitrogen during reproductive stage determining yield. Plant Soil 220:189–205CrossRefGoogle Scholar
  18. Durand N, Briand X, Meyer C (2003) The effect of marine bioactive substance (N PRO) and exogenous cytokinins on nitrate reductase activity in Arabidopsis thaliana. Physiol Plant 119:489–493CrossRefGoogle Scholar
  19. Etienne P, Desclos M, Le Gou L, Gombert J, Bonnefoy J, Maurel K, Le Dily F, Ourry A, Avice JC (2007) N-protein mobilization associated with the leaf senescence process in oilseed rape in concomitant with the disappearance of trypsin inhibitor activity. Funct Plant Biol 34:895–906CrossRefGoogle Scholar
  20. Gardissal CD (1857) A method of treating and preparing seaweeds or marine plants for manure. British Patent vol. XXIX, January–JuneGoogle Scholar
  21. Hervé RA, Roullier DL (1977) Method and apparatus for communiting (sic) marine algae and the resulting product. U.S. Patent 4,023,734Google Scholar
  22. Hong DD, Hien HM, Son PN (2007) Seaweeds from Vietnam used for functional food, medicine and biofertilizer. J Appl Phycol 19:817–826CrossRefGoogle Scholar
  23. Itoh R, Fujiwara M, Nagata N, Yoshida S (2001) A chloroplast protein homologous to the eubacterial topotogical specificity factor MinE plays a role in chloroplast division. Plant Physiol 127:1644–1655PubMedCrossRefGoogle Scholar
  24. Khan W, Rayirath UP, Subramanian S, Jithesh MN, Rayorath P, Hodges DM, Critchley AT, Craigie JS, Norrie J, Prithiviraj B (2009) Seaweed extract as biostimulants of plant growth and development. J Plant Growth Regul 28:386–399Google Scholar
  25. Khan W, Hiltz D, Critchley AT, Prithiviraj B (2011) Bioassay to detect Ascophyllum nodosum extract-induced cytokinin-like activity in Arabidopsis thaliana. J Appl Phycol 23:409–414CrossRefGoogle Scholar
  26. Kojo KH, Fujiwara MT, Itoh RD (2009) Involvement of AtMinE in plastid morphogenesis in various tissues of Arabidopsis thaliana. Biosci Biotechnol Biochem 73:2632–2639PubMedCrossRefGoogle Scholar
  27. Krouk G, Lacombe B, Bielach A, Perrine-Walker F, Malinska K, Mounier E, Hoyerova K, Tillard P, Leon S, Ljung K, Zazimalova E, Benkova E, Nacry P, Gojon A (2010) Nitrate-regulated auxin transport by NRT1.1 defines a mechanism for nutrient sensing in plants. Dev Cell 18:927–937PubMedCrossRefGoogle Scholar
  28. Laîne P, Ourry A, Macduff JH, Boucaud J, Salette J (1993) Kinetic parameters of nitrate uptake by different catch crop species: effects of low temperatures and previous nitrate starvation. Physiol Plant 88:85–92CrossRefGoogle Scholar
  29. Livak KJ, Schmittgen TD (2001) Analysis of gene expression data using real-time quantitative PCR and the 2(-DDc(t)) method. Methods 25:402–408PubMedCrossRefGoogle Scholar
  30. Malagoli P, Laine P, Rossato L, Ourry A (2005) Dynamics of nitrogen uptake and mobilization in field-grown winter oilseed rape (Brassica napus L.) from stem extension to harvest. II A 15N-labelling based simulation model of N partitioning between vegetative and reproductive tissues. Ann Bot 95:1187–1198PubMedCrossRefGoogle Scholar
  31. Mancuso S, Azzarello E, Mugnai S, Briand X(2006) Marine bioactive substance (IPA extract) improve foliar ion uptake and water stress tolerance in potted Vitis vinifera plants. Adv Hortic Sci 20:156–161Google Scholar
  32. Mercier L, Lafitte C, Borderies G, Briand X, Esquerré-Tugayé MT, Fournier J (2001)The algal polysaccharide carrageenans can act as elicitor of plant defense. New Phytol 149:43–51Google Scholar
  33. Matsumoto-Kitano M, Kusumoto T, Tarkowski P, Kinoshita-Tsujimura K, Vaclavikova K, Miyawaki K, Kakimoto T (2008) Cytokinins are central regulator of cambial activity. Proc Natl Acad Sci USA 105:20027–20031PubMedCrossRefGoogle Scholar
  34. Metting B, Rayburn WR, Reynaud PA (1988) Algae and agriculture. In: Lembi C, Waaland JR (eds) Algae and human affairs. Cambridge University Press, New York, pp 335–370Google Scholar
  35. Milton RF (1952) Improvements in or relating to horticultural and agricultural fertilizers. Patent Office London, No. 664:989Google Scholar
  36. Moons A (2005) Regulatory and functional interactions of plant growth regulators and plant glutathione-S-transferase (GSTs). Vitam Horm 72:155–202PubMedCrossRefGoogle Scholar
  37. Mora V, Bacaicoa E, Zamarreno AM, Aguirre E, Garnica M, Fuentes M, Garcia-Mina JM (2010) Action of humic acid on promotion of cucumber shoot growth involves nitrate-related changes associated with the root-to-shoot distribution of cytokinins, polyamines and mineral nutrients. J Plant Physiol 167:633–642PubMedCrossRefGoogle Scholar
  38. Moroney JV, Bartlett SG, Samuelsson G (2001) Carbonic anhydrase in plants and algae. Plant Cell Environ 24:141–153CrossRefGoogle Scholar
  39. Mugnai S, Azzarello E, Pandolfi C, Salamagne S, Briand X, Mancuso S (2008) Enhancement of ammonium and potassium root influxes by the application of marine bioactive substances positively affects Vitis vinifera plant growth. J Appl Phycol 20:177–182CrossRefGoogle Scholar
  40. Nelson WR, Van Staden J (1984) The effect of seaweed concentrate on the growth of nutrient-stressed, greenhouse cucumbers. Hortic Sci 19:81–82Google Scholar
  41. Ohkama N, Takei K, Sakakibara H, Hayashi H, Yoneyama T, Fujiwara T (2002) Regulation of sulfur responsive gene expression by exogenously applied cytokinins in Arabidopsis thaliana. Plant Cell Physiol 43:1493–1501PubMedCrossRefGoogle Scholar
  42. Okazaki K, Kabeya Y, Suzuki K, Mori T, Ichikawa T, Matsui M, Nakanishi H, Miyagishima S (2009) The PLASTID DIVISION 1 and 2 components of the chloroplast division machinery determine the rate of chloroplast division in land plant cell differentiation. Plant Cell 21:1769–1780PubMedCrossRefGoogle Scholar
  43. Ougham HJ, Thomas AM, Thomas BJ, Frick GA, Armstrong GA (2001) Both light-dependent protochlorophyllide oxidoreductase A and protochlorophyllide oxidoreductase B are down-regulated in the slender mutant of barley. J Exp Bot 360:1447–1454CrossRefGoogle Scholar
  44. Park SY, Yu JW, Li J, Yoo SC, Lee NY, Lee SK, Jeong SW, Seo HS, Koh HJ (2007) The senescence-induced staygreen protein regulates chlorophyll degradation. Plant Cell 19:1649–1664PubMedCrossRefGoogle Scholar
  45. Ramanan R, Kannan K, Vinayagamoorthy N, Ramkumar KM, Sivanesan SD, Chakrabarti T (2009) Purification and characterization of a novel plant-type carbonic anhydrase from Bacillus subtilis. Biotechnol Bioprocess Eng 14:32–37CrossRefGoogle Scholar
  46. Rathore SS, Chaudhary DR, Boricha GN, Ghosh A, Bhatt BP, Zodape ST, Patolia JS (2009) Effect of seaweed extract on the growth, yield and nutrient uptake of soybean (Glycine max) under rainfed conditions. S Afr J Bot 75:351–355CrossRefGoogle Scholar
  47. Rayorath P, Jithesh MN, Farid A, Khan W, Palanisamy R, Hankins SD, Critchley AT, Prithiviraj B (2008) Rapid bioassay to evaluate the plant growth promoting activity of Ascophyllum nodosum (L.) Le Jol. using a model plant, Arabidopsis thaliana (L.) Heynh. J Appl Phycol 20:423–429CrossRefGoogle Scholar
  48. Rossato L, Lainé P, Ourry A (2001) Nitrogen storage and remobilization in Brassica napus L. during the growth cycle: nitrogen fluxes within the plant and changes in soluble protein patterns. J Exp Bot 52:1655–1663PubMedCrossRefGoogle Scholar
  49. Roussos PA, Denaka NK, Damvakaris T (2009) Strawberry fruit quality attributes after application of plant growth stimulating compounds. Sci Hortic (Amsterdam) 119:138–146CrossRefGoogle Scholar
  50. Sivasankari S, Venkatesalu V, Anantharaj M, Chandrasekaran M (2006) Effect of seaweed extracts on the growth and biochemical constituents of Vigna sinensis. Bioresour Technol 97:1745–1751PubMedCrossRefGoogle Scholar
  51. Smart CM (1994) Gene expression during leaf senescence. New Phytol 126:419–448CrossRefGoogle Scholar
  52. Spinelli F, Fiori G, Noferini M, Sprocatti M, Costa G (2010) A novel type of seaweed extract as a natural alternative to the use of iron chelates in strawberry production. SciHortic (Amsterdam) 125:263–269CrossRefGoogle Scholar
  53. Temple WD, Bomke AA (1988) Effects of kelp (Macrocystis integrifolia) on soil chemical properties and crop responses. Plant Soil 105:213–222CrossRefGoogle Scholar
  54. Turan M, Köse C (2004) Seaweed extracts improve copper uptake of grapevine. Acta Agr Scand B 54:213–220Google Scholar
  55. Vaughan DA, Balazs E, Heslop-Harrison JS (2007) From crop domestication to super-domestication. Ann Bot 100:893–901PubMedCrossRefGoogle Scholar
  56. Zavaleta-Mancera HA, Lopez-Delgado H, Loza-Tavera H, Mora-Herrera M, Trevilla-Garcia C, Vargas-Suarez M, Ougham H (2007) Cytokinin promotes catalase and ascorbate peroxidase activities and preserves the chloroplast integrity during dark-senescence. J Plant Physiol 164:1572–1582PubMedCrossRefGoogle Scholar
  57. Zhang X, Schmidt RE (1997) The impact of growth regulators on the α-tocopherol status in water-stressed Poa pratensis. Int Turfgrass Soc Res J 8:1364–1371Google Scholar

Copyright information

© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  • Laëtitia Jannin
    • 1
  • Mustapha Arkoun
    • 1
  • Philippe Etienne
    • 1
  • Philippe Laîné
    • 1
  • Didier Goux
    • 2
  • Maria Garnica
    • 3
  • Marta Fuentes
    • 3
  • Sara San Francisco
    • 3
  • Roberto Baigorri
    • 3
  • Florence Cruz
    • 4
  • Fabrice Houdusse
    • 4
  • José-Maria Garcia-Mina
    • 3
  • Jean-Claude Yvin
    • 4
  • Alain Ourry
    • 1
    Email author
  1. 1.UMR 950 Ecophysiologie Végétale, Agronomie et nutritions N, C, S, Esplanade de la paixUniversité de Caen Basse-Normandie et INRACaen CedexFrance
  2. 2.Centre de Microscopie Appliquée à la Biologie (CMABio), Esplanade de la PaixUniversité de Caen Basse-NormandieCaen CedexFrance
  3. 3.TIMAC Agro Spain, CIPAV, Groupe Roullier, Poligono de Arazuri-OrcoyenOrcoyenSpain
  4. 4.Centre de Recherche International en Agroscience, CRIAS-TAI, Groupe RoullierDinardFrance

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