Advertisement

External Supplement of Impulsive Micromanager Trichoderma Helps in Combating CO2 Stress in Rice Grown Under FACE

  • Aradhana Mishra
  • Satyendra Pratap Singh
  • Sahil Mahfooz
  • Richa Shukla
  • Nishtha Mishra
  • Shipra Pandey
  • Sanjay Dwivedi
  • Vivek Pandey
  • Pramod Arvind Shirke
  • Chandra Shekhar Nautiyal
Original Paper
  • 42 Downloads

Abstract

The present study aims to explore the alternative way to improve the quality and productivity of rice grown under CO2 stress through an external supplement of Trichoderma as a biofertilizer (BF). The impact of BF-treated rice under elevated CO2 (eCO2) was examined by different plant growth parameters, physiological observations, scanning electron microscopy, microbial community profiling and expression levels of stress-related genes. The effect of eCO2 on percent change in yielding attributes of rice (Heena and Kiran) was found higher in control, whereas it was reduced in the presence of BF. Photosynthetic rate, stomatal conductance and transpiration rate were higher in BF-treated rice under eCO2 condition. SEM analysis of BF-treated roots exhibits an increase in the number of metaxylem along with its diameter with thicker and rigid sclerenchymatous cells. Expression analysis of stress-related genes showed an increase in their mRNA transcripts under eCO2 condition. A significant change in the microbial community was found in the rhizospheric region of Heena treated with BF under eCO2. The current study demonstrates the potential of BF in ameliorating the stress generated as a result of CO2 enrichment.

Keywords

Elevated CO2 FACE Microbial diversity SEM Stress genes T. reesei 

Notes

Acknowledgments

The authors are grateful to Dr. P. N. Saxena (CSIR-Indian Institute of Toxicology Research, Lucknow) for SEM micrograph imaging.

Funding Information

This work is supported by funding from Science and Engineering Research Board, New Delhi (GAP3349), and Council of Scientific and Industrial Research (PSC0112).

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no competing interest

Supplementary material

11105_2018_1133_MOESM1_ESM.doc (40 kb)
ESM 1 (DOC 41 kb)

References

  1. Abdelrahman M, Abdel-Motaal F, El-Sayed M, Jogaiah S, Shigyo M, Ito S, Tran LS (2016) Dissection of Trichoderma longibrachiatum-induced defense in onion (Allium cepa L.) against Fusarium oxysporum f. sp. cepa by target metabolite profiling. Pl Sci 246:128–138CrossRefGoogle Scholar
  2. Agrawal L, Gupta S, Mishra SK, Pandey G, Kumar S, Chauhan PS, Chakrabarty D, Nautiyal CS (2016) Elucidation of complex nature of PEG induced drought-stress response in Rice root using comparative proteomics approach. Front Plant Sci 7:1466.  https://doi.org/10.3389/fpls.2016.01466 CrossRefPubMedPubMedCentralGoogle Scholar
  3. Ahmad P, Hashem A, Abd-Allah EF, Alqarawi AA, John R, Egamberdieva D, Gucel S (2015) Role of Trichoderma harzianum in mitigating NaCl stress in Indian mustard (Brassica juncea L) through antioxidative defense system. Front Pl Sci 6:868Google Scholar
  4. Ainsworth EA, Long SP (2005) What have we learned from 15 years of free-air CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy. New Phytol 165:351–371CrossRefGoogle Scholar
  5. Albrecht-Gary AM, Crumbliss AL (1998) Coordination chemistry of siderophores: thermodynamics and kinetics of iron chelation and release. Metal Ions Bio Sys 35:239–327Google Scholar
  6. Alcantara C, Thornton CR, Perez-de-Luque A, Le Cocq K, Pedraza V, Murray PJ (2016) The free-living rhizosphere fungus Trichoderma hamatum GD12 enhances clover productivity in clover-ryegrass mixtures. Plant Soil 398:165–180CrossRefGoogle Scholar
  7. Amara I, Capellades M, Ludevid MD, Pages M, Goday A (2013) Enhanced water stress tolerance of transgenic maize plants over-expressing LEA Rab28 gene. J Plant Physiol 170:864–873CrossRefGoogle Scholar
  8. Bae H, Roberts DP, Lim HS, Strem MD, Park SC, Ryu CM, Melnick RL, Bailey BA (2011) Endophytic Trichoderma isolates from tropical environments delay disease onset and induce resistance against Phytophthora capsici in hot pepper using multiple mechanisms. Mol Plant Microbe In 24:336–351CrossRefGoogle Scholar
  9. Blagodatskaya E, Blagodatsky S, Dorodnikov M, Kuzyakov Y (2010) Elevated atmospheric CO2 increases microbial growth rates in soil: results of three CO2 enrichment experiments. Global C Biol 16:836–848CrossRefGoogle Scholar
  10. Blokhina O, Virolainen E, Fagerstedt KV (2003) Antioxidants, oxidative damage and oxygen deprivation stress: a review. Ann Bot-London 91:179–194CrossRefGoogle Scholar
  11. Brotman Y, Landau U, Cuadros-Inostroza A, Tohge T, Fernie AR, Chet I, Viterbo A, Willmitzer L (2013) Trichoderma-plant root colonization: escaping early plant defense responses and activation of the antioxidant machinery for saline stress tolerance. PLoS Patho 9:e1003221CrossRefGoogle Scholar
  12. Contreras-Cornejo HA, Macias-Rodriguez L, Alfaro-Cuevas R, Lopez-Bucio J (2014) Trichoderma spp. improve growth of Arabidopsis seedlings under salt stress through enhanced root development, Osmolite production, and Na+ elimination through root exudates. Mol Plant Microbe In 27:503–514CrossRefGoogle Scholar
  13. Contreras-Cornejo HA, Macias-Rodriguez L, Del-Val E, Larsen J (2016) Ecological functions of Trichoderma spp. and their secondary metabolites in the rhizosphere: interactions with plants. FEMS Microbiol Ecol 92(4):1–17CrossRefGoogle Scholar
  14. Contreras-Cornejo HA, Macias-Rodriguez L, Vergara AG, Lopez-Bucio J (2015) Trichoderma modulates stomatal aperture and leaf transpiration through an abscisic acid-dependent mechanism in Arabidopsis. J Plant Growth Regul 34:425–432CrossRefGoogle Scholar
  15. Dixon DP, Davis BG, Edwards R (2002) Functional divergence in the glutathione transferase superfamily in plants - Identification of two classes with putative functions in redox homeostasis in Arabidopsis thaliana. J Biol Chem 277:30859–30869CrossRefGoogle Scholar
  16. FAO (2015) FAO Rice Market Monitor.Google Scholar
  17. Edwards R, Dixon DP, Walbot V (2000) Plant glutathione S-transferases: enzymes with multiple functions in sickness and in health. Trends Plant Sci 5:193–198CrossRefGoogle Scholar
  18. Gao J, Lan T (2016) Functional characterization of the late embryogenesis abundant (LEA) protein gene family from Pinus tabuliformis (Pinaceae) in Escherichia coli. Sci Rep 6:19467CrossRefGoogle Scholar
  19. Garland JL (1996) Patterns of potential C source utilization by rhizosphere communities. Soil Biol Biochem 28:223–230CrossRefGoogle Scholar
  20. Garland JL, Mills AL (1991) Classification and characterization of heterotrophic microbial communities on the basis of patterns of community-level sole-carbon-source utilization. Appl Environ Microbiol 57:2351–2359PubMedPubMedCentralGoogle Scholar
  21. Greve K, La Cour TJ, Poulsen MK, FM Skriver K (2003) Interactions between plant RING-H2 and plant-specific NAC (NAM/ATAF1/2/CUC2) proteins: RING-H2 molecular specificity and cellular localization. Biochem J 371:97–108CrossRefGoogle Scholar
  22. Guo J, Zhang MQ, Wang XW, Zhang WJ (2015) Elevated CO2 facilitates C and N accumulation in a rice paddy ecosystem. J Environ Sci-China 29:27–33CrossRefGoogle Scholar
  23. Hanin M, Brini F, Ebel C, Toda Y, Takeda S, Masmoudi K (2011) Plant dehydrins and stress tolerance: versatile proteins for complex mechanisms. Pl Sig Behv 6:1503–1509CrossRefGoogle Scholar
  24. Hirasawa T, Iida Y, Ishihara K (1988) Effect of leaf water potential and air humidity on photosynthetic rate and diffusive conductance in Rice plants. Jpn J Crop Sci 57:112–118CrossRefGoogle Scholar
  25. Hodge A (1996) Impact of elevated CO2 on mycorrhizal associations and implications for plant growth. Biol Fert Soils 23:388–398CrossRefGoogle Scholar
  26. IPCC (2014) In: Edenhofer, O, R, P-M, Sokona Y, FE, S Kadner, S, A Adler, BI, BrunnerS, B, EP, Kriemann J, Savolainen S, Schlomer C von Stechow, Zwickel T, Minx JC (Eds), Mitigation of Climate Change. Contribution of Working Group III to the Fifth Assessment Report of the Intergovernmental Panel on Climate ChangeGoogle Scholar
  27. Jensen MK, Kjaersgaard T, Nielsen MM, Galberg P, Petersen K, O'Shea C, Skriver K (2010) The Arabidopsis thaliana NAC transcription factor family: structure-function relationships and determinants of ANAC019 stress signalling. Biochem J 426:183–196CrossRefGoogle Scholar
  28. Kanerva T, Palojarvi A, Ramo K, Manninen S (2008) Changes in soil microbial community structure under elevated tropospheric O−3 and CO2. Soil Biol Biochem 40:2502–2510CrossRefGoogle Scholar
  29. Kusumi K, Hirotsuka S, Kumamaru T, Iba K (2012) Increased leaf photosynthesis caused by elevated stomatal conductance in a rice mutant deficient in SLAC1, a guard cell anion channel protein. J Exp Bot 63:5635–5644CrossRefGoogle Scholar
  30. Lesaulnier C, Papamichail D, McCorkle S, Ollivier B, Skiena S, Taghavi S, Zak D, van der Lelie D (2008) Elevated atmospheric CO2 affects soil microbial diversity associated with trembling aspen. Environ Microbiol 10:926–941CrossRefGoogle Scholar
  31. Li RX, Cai F, Pang G, Shen QR, Li R, Chen W (2015) Solubilisation of phosphate and micronutrients by Trichoderma harzianum and its relationship with the promotion of tomato plant growth. PLoS One 10Google Scholar
  32. Liu Y, Xie L, Liang X, Zhang S (2015) CpLEA5, the late embryogenesis abundant protein gene from Chimonanthus praecox, possesses low temperature and osmotic resistances in prokaryote and eukaryotes. Int J Mol Sci 16:26978–26990CrossRefGoogle Scholar
  33. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(T)(−Delta Delta C) method. Methods 25:402–408CrossRefGoogle Scholar
  34. Loukehaich R, Wang TT, Ouyang B, Ziaf K, Li HX, Zhang JH, Lu YE, Ye ZB (2012) SpUSP, an annexin-interacting universal stress protein, enhances drought tolerance in tomato. J Exp Bot 63:5593–5606CrossRefGoogle Scholar
  35. Lugtenberg B, Kamilova F (2009) Plant-growth-promoting rhizobacteria. Annual Rev Microb 63:541–556CrossRefGoogle Scholar
  36. Mahfooz S, Singh SP, Rakh R, Bhattacharya A, Mishra N, Singh PC, Chauhan PS, Nautiyal CS, Mishra A (2016) A comprehensive characterization of simple sequence repeats in the sequenced Trichoderma genomes provides valuable resources for marker development. Frontiers in Microbiol 7:1–11CrossRefGoogle Scholar
  37. Mastouri F, Bjorkman T, Harman GE (2010) Seed treatment with Trichoderma harzianum alleviates biotic, abiotic, and physiological stresses in germinating seeds and seedlings. Phytopathology 100:1213–1221CrossRefGoogle Scholar
  38. Mishra A, Kumari M, Pandey S, Chaudhry V, Gupta KC, Nautiyal CS (2014) Biocatalytic and antimicrobial activities of gold nanoparticles synthesized by Trichoderma sp. Bioresour Technol 166:235–242CrossRefGoogle Scholar
  39. Mishra A, Nautiyal CS (2009) Functional diversity of the microbial community in the rhizosphere of chickpea grown in diesel fuel-spiked soil amended with Trichoderma ressei using sole-carbon-source utilization profiles. World J Microbiol Biotechnol 25:1175–1180CrossRefGoogle Scholar
  40. Mishra A, Nautiyal CS (2013) A novel recombinant strain of Trichoderma useful for enhancing nutritional value and growth of plantsGoogle Scholar
  41. Nautiyal CS (2009) Self-Purificatory ganga water facilitates death of pathogenic Escherichia coli O157:H7. Current Microbiol 58:25–29CrossRefGoogle Scholar
  42. Nishimura A, Ito M, Kamiya N, Sato Y, Matsuoka M (2002) OsPNH1 regulates leaf development and maintenance of the shoot apical meristem in rice. Plant J 30:189–201CrossRefGoogle Scholar
  43. Okubo T, Liu DY, Tsurumaru H, Ikeda S, Asakawa S, Tokida T, Tago K, Hayatsu M, Aoki N, Ishimaru K, Ujiie K, Usui Y, Nakamura H, Sakai H, Hayashi K, Hasegawa T, Minamisawa K (2015) Elevated atmospheric CO2 levels affect community structure of rice root-associated bacteria. Frontiers in Microbiol 6Google Scholar
  44. Pandey V, Ansari MW, Tula S, Yadav S, Sahoo RK, Shukla N, Bains G, Badal S, Chandra S, Gaur AK, Kumar A, Shukla A, Kumar J, Tuteja N (2016) Dose-dependent response of Trichoderma harzianum in improving drought tolerance in rice genotypes. Planta 243:1251–1264CrossRefGoogle Scholar
  45. Pathan AK, Bond J, Gaskin RE (2010) Sample preparation for SEM of plant surfaces. Mater Today 12:32–43CrossRefGoogle Scholar
  46. Rêgo M, Borges F, Filippi M, Gonçalves L, Silva G (2014) Morphoanatomical and biochemical changes in the roots of Rice plants induced by plant growth-promoting microorganisms. Journal of Bot 2014Google Scholar
  47. Rillig MC, Wright SF, Shaw MR, Field CB (2002) Artificial climate warming positively affects arbuscular mycorrhizae but decreases soil aggregate water stability in an annual grassland. Oikos 97:52–58CrossRefGoogle Scholar
  48. Roberts DP, Maul JE, McKenna LF, Emche SE, Meyer SLF, Collins RT, Bowers JH (2010) Selection of genetically diverse Trichoderma spp. isolates for suppression of Phytophthora capsici on bell pepper. Canadian J Microbiol 56:864–873CrossRefGoogle Scholar
  49. Salleh FM, Evans K, Goodall B, Machin H, Mowla SB, Mur LA, Runions J, Theodoulou FL, Foyer CH, Rogers HJ (2012) A novel function for a redox-related LEA protein (SAG21/AtLEA5) in root development and biotic stress responses. Pl Cell Environ 35:418–429CrossRefGoogle Scholar
  50. Samolski I, Rincon AM, Pinzon LM, Viterbo A, Monte E (2012) The qid74 gene from Trichoderma harzianum has a role in root architecture and plant biofertilization. Microbiol-Sgm 158:129–138CrossRefGoogle Scholar
  51. Sharma R, Sahoo A, Devendran R, Jain M (2014) Over-expression of a rice tau class glutathione s-transferase gene improves tolerance to salinity and oxidative stresses in Arabidopsis. PLoS One 9:e92900CrossRefGoogle Scholar
  52. Shinde S, Behpouri A, McElwain JC, Ng CKY (2015) Genome-wide transcriptomic analysis of the effects of sub-ambient atmospheric oxygen and elevated atmospheric carbon dioxide levels on gametophytes of the moss, Physcomitrella patens. J Experimental Bot 66:4001–4012CrossRefGoogle Scholar
  53. Shukla N, Awasthi RP, Rawat L, Kumar J (2012) Biochemical and physiological responses of rice (Oryza sativa L.) as influenced by Trichoderma harzianum under drought stress. Plant Physiol Bioch 54:78–88CrossRefGoogle Scholar
  54. Staddon PL, Heinemeyer A, Fitter AH (2002) Mycorrhizas and global environmental change: research at different scales. Plant Soil 244:253–261CrossRefGoogle Scholar
  55. Tripathi P, Singh PC, Mishra A, Tripathi RD, Nautiyal CS (2015) Trichoderma inoculation augments grain amino acids and mineral nutrients by modulating arsenic speciation and accumulation in chickpea (Cicer arietinum L.). Ecotox Environ Safe 117:72–80CrossRefGoogle Scholar
  56. Usui Y, Sakai H, Tokida T, Nakamura H, Nakagawa H, Hasegawa T (2015) Rice grain yield and quality responses to free-air CO enrichment combined with soil and water warming. Glob Chang Biol 22:1256–1270CrossRefGoogle Scholar
  57. Wang JY, Wang C, Chen NN, Xiong ZQ, Wolfe D, Zou JW (2015) Response of rice production to elevated [CO2] and its interaction with rising temperature or nitrogen supply: a meta-analysis. Clim Chang 130:529–543CrossRefGoogle Scholar
  58. Yang LX, Huang JY, Yang HJ, Zhu JG, Liu HJ, Dong GC, Liu G, Han Y, Wang YL (2006) The impact of free-air CO2 enrichment (FACE) and N supply on yield formation of rice crops with large panicle. Field Crop Res 98:141–150CrossRefGoogle Scholar
  59. Zak DR, Pregitzer KS, King JS, Holmes WE (2000) Elevated atmospheric CO2, fine roots and the response of soil microorganisms: a review and hypothesis. New Phytol 147:201–222CrossRefGoogle Scholar
  60. Zhu CW, Xu X, Wang D, Zhu JG, Liu G (2015) An indica rice genotype showed a similar yield enhancement to that of hybrid rice under free air carbon dioxide enrichment (vol 5, 12719, 2015). Sci Rep-Uk:5Google Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Aradhana Mishra
    • 1
  • Satyendra Pratap Singh
    • 1
  • Sahil Mahfooz
    • 1
  • Richa Shukla
    • 1
  • Nishtha Mishra
    • 1
  • Shipra Pandey
    • 1
  • Sanjay Dwivedi
    • 2
  • Vivek Pandey
    • 3
  • Pramod Arvind Shirke
    • 3
  • Chandra Shekhar Nautiyal
    • 1
  1. 1.Division of Plant Microbe InteractionsCSIR-National Botanical Research InstituteLucknowIndia
  2. 2.Division of Plant Ecology and Environmental SciencesCSIR-National Botanical Research InstituteLucknowIndia
  3. 3.Plant Physiology LabCSIR-National Botanical Research InstituteLucknowIndia

Personalised recommendations