Advertisement

Changes in growth and soil microbial communities in reciprocal grafting clones between Populus deltoides males and females exposed to water deficit conditions

  • 51 Accesses

Abstract

Key message

Our findings highlight that male-rooted clones (M/M and F/M) of Populus deltoides are more water-deficit tolerant than female-rooted clones (F/F and M/F), as shown by a smaller decrease in total biomass and net photosynthetic rate in the male-rooted clones.

Context

It has been reported that graft clones (female scion and male rootstock) in poplars may be an option to mitigate the effects of water deficit on plants. However, the extent to which grafting mitigates the effect of soil water deficit on soil microorganisms remains poorly understood.

Aims

The research was designed to investigate the effects of soil water deficit on plant growth, soil microbial communities, and soil enzymatic activities of the reciprocal graft clones of P. deltoides.

Methods

Four different graft clones (female shoot scion and female rootstock, F/F; male shoot scion and female rootstock, M/F; male shoot scion and male rootstock scion, M/M; and female shoot scion and male rootstock, F/M) in P. deltoides were used. Two watering regimes, irrigation and soil water deficit (i.e., non-irrigation conditions, natural levels of precipitation) were included in the experiments. The microbial community structure was quantified using phospholipid fatty acid.

Results

Under water deficit, the decreases in total biomass, net photosynthetic rates, and leaf nitrogen content were more evident in M/M and F/M than in F/F and M/F. Bacterial phospholipid fatty acids (PLFAs) and actinomycetal PLFAs remained unaffected in the four graft clones. In contrast, during soil water deficit, fungal PLFAs were higher in M/M and F/M soil coincided with higher extracellular activities of β-1,4-N-acetyl-glucosaminidase and leucine aminopeptidase.

Conclusion

Male-rooted clones (M/M and F/M) are more tolerant to water deficit than female-rooted clones (F/F and M/F). It is possible that the better performance of M/M and F/M, when exposed to water deficit, is associated mainly with higher fine root activity, greater specific root length and root/shoot ratio as well as increased fungal PLFAs.

This is a preview of subscription content, log in to check access.

Access options

Buy single article

Instant unlimited access to the full article PDF.

US$ 39.95

Price includes VAT for USA

Subscribe to journal

Immediate online access to all issues from 2019. Subscription will auto renew annually.

US$ 99

This is the net price. Taxes to be calculated in checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Data availability

The datasets generated and analyzed during the current study are available from the corresponding author on reasonable request.

References

  1. Allen CD, Macalady AK, Chenchouni H, Bachelet D, McDowell N, Vennetier M, Kitzberger T, Rigling A, Breshears DD, Hogg EH, Gonzalez P, Fensham R, Zhang Z, Castro J, Demidova N, Lim JH, Allard G, Running SW, Semerci A, Cobb N (2010) A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. For Ecol Manag 259:660–684

  2. Basile B, Bryla DR, Salsman ML, Marsal J, Cirillo C, Johnson RS, DeJong TM (2007) Growth patterns and morphology of fine roots of size-controlling and invigorating peach rootstocks. Tree Physiol 27:231–241

  3. Cantero-Navarro E, Romero-Aranda R, Fernández-Muñoz R, Martínez-Andújar C, Pérez-Alfocea F, Albacete A (2016) Improving agronomic water use efficiency in tomato by rootstock-mediated hormonal regulation of leaf biomass. Plant Sci 251:90–100

  4. Chapin FS, Autumn K, Pugnaire F (1993) Evolution of suites of traits in response to environmental stress. Am Nat 142:S78–S92

  5. Ciais P, Reichstein M, Viovy N, Granier A, Ogee J, Allard V, Aubinet M, Buchmann N, Bernhofer C, Carrara A, Chevallier F, De Noblet N, Friend AD, Friedlingstein P, Grunwald T, Heinesch B, Keronen P, Knohl A, Krinner G, Loustau D, Manca G, Matteucci G, Miglietta F, Ourcival JM, Papale D, Pilegaard K, Rambal S, Seufert G, Soussana JF, Sanz MJ, Schulze ED, Vesala T, Valentini R (2005) Europe-wide reduction in primary productivity caused by the heat and drought in 2003. Nature 437:529–533

  6. Colla G, Rouphael Y, Cardarelli M, Salerno A, Rea E (2010) The effectiveness of grafting to improve alkalinity tolerance in watermelon. Environ Exp Bot 68:283–291

  7. Comas LH, Mueller KE, Taylor LL, Midford PE, Callahan HS, Beerling DJ (2012) Evolutionary patterns and biogeochemical significance of angiosperm root traits. Int J Plant Sci 173:584–595

  8. Darwent MJ (2003) Biosensor reporting of root exudation from Hordeum vulgare in relation to shoot nitrate concentration. J Exp Bot 54:325–334

  9. De Vries FT, Shade A (2013) Controls on soil microbial community stability under climate change. Front Microbiol 4:265

  10. Erismann ND, Machado EC, Tucci MLS (2008) Photosynthetic limitation by CO2 diffusion in drought stressed orange leaves on three rootstocks. Photosynth Res 96:163–172

  11. Federle TW (1986) Microbial distribution in the soil-new techniques. In: Megusar F, Gantar M (eds) Perspectives in microbial ecology. Slovene Society for Microbiology, Ljubljana, pp 493–498

  12. Fender AC, Gansert D, Jungkunst HF, Fiedler S, Beyer F, Schützenmeister K, Thiele B, Valtanen K, Polle A, Leuschner C (2013) Root-induced tree species effects on the source/sink strength for greenhouse gases (CH4, N2O and CO2) of a temperate deciduous forest soil. Soil Biol Biochem 57:587–597

  13. Feng XJ, Simpson AJ, Schilesinger WH, Simpson MJ (2010) Altered microbial community structure and organic matter composition under elevated CO2 and N fertilization in the Duke forest. Glob Chang Biol 16:2104–2116

  14. Frostegård Å, Tunlidb A, Bååth E (1991) Microbial biomass measured as total lipid phosphate in soils of different organic content. J Microbiol Methods 14:151–163

  15. Frostegård Å., Tunlidb A, Bååth E (1993) Phospholipid fatty acid composition, biomass, and activity of microbial communities from two soil types experimentally exposed to different heavy metals. Appl Environ Microbiol 59:3605–3617

  16. Fuchslueger L, Bahn M, Fritz K, Hasibeder R, Richter A (2014) Experimental drought reduces the transfer of recently fixed plant carbon to soil microbes and alters the bacterial community composition in a mountain meadow. New Phytol 201:916–927

  17. Gao Y, Tian Y, Liang X, Gao L (2015) Effects of single-root-grafting, double-root-grafting and compost application on microbial properties of rhizosphere soils in Chinese protected cucumber (Cucumis sativus L.) production systems. Sci Hortic 186:190–200

  18. Han QQ, Luo JX, Li ZJ, Korpelainen H, Li CY (2018) Improved drought resistance by intergeneric grafting in Salicaceae plants under water deficits. Environ Exp Bot 155:217–225

  19. Han Y, Wang Y, Jiang H, Wang M, Korpelainen H, Li C (2013) Reciprocal grafting separates the roles of the root and shoot in sex-related drought responses in Populus cathayana males and females. Plant Cell Environ 36:356–364

  20. Hawkes CV, Kivlin SN, Rocca JD, Huguet V, Thomsen MA, Suttle KB (2011) Fungal community responses to precipitation. Glob Chang Biol 17:1637–1645

  21. Hernández EI, Vilagrosa A, Pausas JG, Bellot J (2010) Morphological traits and water use strategies in seedlings of Mediterranean coexisting species. Plant Ecol 207:233–244

  22. Hobbie E, Ouimette A (2009) Controls of nitrogen isotope patterns in soil profiles. Biogeochemistry 95:355–371

  23. Högberg P (1997) 15N natural abundance in soil-plant systems. New Phytol 137:179–203

  24. Huang Z, Wan X, He Z, Yu Z, Wang M, Hu Z, Yang Y (2013) Soil microbial biomass, community composition and soil nitrogen cycling in relation to tree species in subtropical China. Soil Biol Biochem 62:68–75

  25. Huang Z, Xu Z, Chen C (2008) Effect of mulching on labile soil organic matter pools, microbial community functional diversity and nitrogen transformations in two hardwood plantations of subtropical Australia. Appl Soil Ecol 40:229–239

  26. Kanerva T, Palojärvi A, Rämö K, Manninen S (2008) Changes in soil microbial community structure under elevated tropospheric O3 and CO2. Soil Biol Biochem 40:2502–2510

  27. Karlowsky S, Augusti A, Ingrisch J, Hasibeder R, Lange M, Lavorel S, Bahn M, Gleixner G (2018) Land use in mountain grasslands alters drought response and recovery of carbon allocation and plant-microbial interactions. J Ecol 106:1230–1243

  28. Lemoine R, La Camera S, Atanassova R, Dedaldechamp F, Allario T, Pourtau N, Bonnemain JL, Laloi M, Coutos-Thevenot P, Maurousset L, Faucher M, Girousse C, Lemonnier P, Parrilla J, Durand M (2013) Source-to-sink transport of sugar and regulation by environmental factors. Front Plant Sci 4:272

  29. Li Y, Duan B, Chen J, Korpelainen H, Niinemets Ü, Li C (2016) Males exhibit competitive advantages over females of Populus deltoides under salinity stress. Tree Physiol 12:1573–1584

  30. Louws FJ, Rivard CL, Kubota C (2010) Grafting fruiting vegetables to manage soilborne pathogens, foliar pathogens, arthropods and weeds. Sci Hortic 127:127–146

  31. Machado DFSP, Ribeiro RV, Silveira JAG, Magalhães Filho JR, Machado EC (2013) Rootstocks induce contrasting photosynthetic responses of orange plants to low night temperature without affecting the antioxidant metabolism. Theor Exp Plant Physiol 25:26–35

  32. Manzoni S, Schimel J, Porporato A (2012) Responses of soil microbial communities to water stress: results from a meta-analysis. Ecology 93:930–938

  33. Mariotte P, Robroek BJM, Jassey VEJ, Buttler A (2015) Subordinate plants mitigate drought effects on soil ecosystem processes by stimulating fungi. Funct Ecol 29:1578–1586

  34. Martínez-Ballesta MC, Alcaraz-López C, Muries B, Mota-Cadenas C, Carvajal M (2010) Physiological aspects of rootstock-scion interactions. Sci Hortic 127:112–118

  35. Martinez-Rodriguez MM, Estan MT, Moyano E, Garcia-Abellan JO, Flores FB, Campos JF, Al-Azzawi MJ, Flowers TJ, Bolarin MC (2008) The effectiveness of grafting to improve salt tolerance in tomato when an ‘excluder’ genotype is used as scion. Environ Exp Bot 63:392–401

  36. Mauclaire L, Pelz O, Thullner M, Abraham W, Zeyer J (2003) Assimilation of toluene carbon along a bacteria-protist food chain determined by 13C-enrichment of biomarker fatty acids. J Microbiol Methods 55:635–649

  37. McGuire KL, Bent E, Borneman J, Majumder A, Allison SD, Treseder KK (2010) Functional diversity in resource use by fungi. Ecology 91:2324–2233

  38. Miller SS, Driscoll BT, Gregerson RG, Gantt JS, Vance CP (1998) Alfalfa malate dehydrogenase MDH: molecular cloning and characterization of five different forms reveals a unique nodule-enhanced MDH. Plant J 15:173–184

  39. O'Leary WM, Wilkinson SG (1988) Gram-positive bacteria. In: Ratledge C, Wilkinson SG (eds) Microbial lipids, vol 1. Academic, London, pp 117–202

  40. Passioura J (2007) The drought environment: physical, biological and agricultural perspectives. J Exp Bot 58:113–117

  41. Passioura JB (2002) Environmental biology and crop improvement. Funct Plant Biol 29:53–546

  42. Paterson E, Midwood AJ, Millard P (2009) Through the eye of the needle: a review of isotope approaches to quantify microbial processes mediating soil carbon balance. New Phytol 184:19–33

  43. Phillips RP, Meier IC, Bernhardt ES, Grandy AS, Wickings K, Finzi AC (2012) Roots and fungi accelerate carbon and nitrogen cycling in forests exposed to elevated CO2. Ecol Lett 15:1042–1049

  44. Rodríguez-Gamir J, Primo-Millo E, Forner JB, Forner-Giner MA (2010) Citrus rootstock responses to water stress. Sci Hortic 126:95–102

  45. Rouphael Y, Cardarelli M, Rea E, Colla G (2008) Grafting of cucumber as a means to minimize copper toxicity. Environ Exp Bot 63:49–58

  46. Royer-Tardif S, Bradley RL, Parsons WFJ (2010) Evidence that plant diversity and site productivity confer stability to forest floor microbial biomass. Soil Biol Biochem 42:813–821

  47. Saiya-Cork KR, Sinsabaugh RL, Zak DR (2002) The effects of long term nitrogen deposition on extracellular enzyme activity in an Acer saccharum forest soil. Soil Biol Biochem 34:1309–1315

  48. Scheffers BR, De Meester L, Bridge TCL, Hoffmann AA, Pandolfi JM, Corlett RT, Butchart SHM, Pearce-Kelly P, Kovacs KM, Dudgeon D, Pacifici M, Rondinini C, Foden WB, Martin TG, Mora C, Bickford D, Watson JEM (2016) The broad footprint of climate change from genes to biomes to people. Science 354:aaf7671

  49. Schindlbacher A, Rodler A, Kuffner M, Kitzler B, Sessitsch A, Zechmeister-Boltenstern S (2011) Experimental warming effects on the microbial community of a temperate mountain forest soil. Soil Biol Biochem 43:1417–1425

  50. Schwarz D, Rouphael Y, Colla G, Venema JH (2010) Grafting as a tool to improve tolerance of vegetables to abiotic stresses: thermal stress, water stress and organic pollutants. Sci Hortic 127:162–171

  51. Sixto H, Grau JM, Alba N, Alia R (2005) Response to sodium chloride in different species and clones of genus Populus L. Forestry 78:93–104

  52. Smith DM, Inman-Bamber NG, Thorburn PJ (2005) Growth and function of the sugarcane root system. Field Crop Res 92:169–183

  53. Smith FA, Grace EJ, Smith SE (2009) More than a carbon economy: nutrient trade and ecological sustainability in facultative arbuscular mycorrhizal symbioses. New Phytol 182:347–358

  54. Smithwick EAH, Turner MG, Metzger KL, Balser TC (2005) Variation in NH4+ mineralization and microbial communities with stand age in lodgepole pine (Pinus contorta) forests, Yellowstone National Park (USA). Soil Biol Biochem 37:1546–1559

  55. Steinauer K, Tilman D, Wragg PD, Cesarz S, Cowles JM, Pritsch K, Reich PB, Weisser WW, Eisenhauer N (2015) Plant diversity effects on soil microbial functions and enzymes are stronger than warming in a grassland experiment. Ecology 96:99–112

  56. Tian Y, Zhang X, Liu J, Chen Q, Gao L (2009) Microbial properties of rhizosphere soils as affected by rotation, grafting, and soil sterilization in intensive vegetable production systems. Sci Hortic 123:139–147

  57. Xu W, Cui K, Xu A, Nie L, Huang J, Peng S (2015) Drought stress condition increases root to shoot ratio via alteration of carbohydrate partitioning and enzymatic activity in rice seedlings. Acta Physiol Plant 37:1–11

  58. Xu X, Peng GQ, Wu CC, Korpelainen H, Li CY (2008) Drought inhibits photosynthetic capacity more in females than in males of Populus cathayana. Tree Physiol 28:1751–1759

  59. Xu Z, Chen L, Tang S, Zhuang L, Yang W, Tu L, Tan B, Zhang L (2016) Sex-specific responses to Pb stress in Populus deltoids : root architecture and Pb translocation. Trees 30:2019–2027

  60. Yin H, Li Y, Xiao J, Xu Z, Cheng X, Liu Q (2013) Enhanced root exudation stimulates soil nitrogen transformations in a subalpine coniferous forest under experimental warming. Glob Chang Biol 19:2158–2167

  61. Zhang S, Jiang H, Peng SM, Korpelainen H, Li CY (2011) Sex-related differences in morphological, physiological, and ultrastructural responses of Populus cathayana to chilling. J Exp Bot 62:675–686

  62. Zhao HX, Li Y, Zhang XL, Korpelainen H, Li CY (2012) Sex-related and stage-dependent source-to-sink transition in Populus cathayana grown at elevated CO2 and elevated temperature. Tree Physiol 32:1325–1338

  63. Zhou B, Yin Y, Xu Y, Han L, Ye X, Bai L (2010) Effect of grafting on rhizospheric soil microorganisms and leaf NR activities of eggplants. Acta Hortic Sin 37:53–58

Download references

Author information

Correspondence to Baoli Duan.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Contribution of the co-authors

Weilong Liu led the manuscript preparation with substantial contributions from all the coauthors. Yanping Wang, Xu Gong and Shuxin Li contributed substantially to the data collection. Joseph M. Smoak contributed significantly to the critical revisions of the manuscript. Baoli Duan supervised the research work and revised the manuscript. All authors read and approved the final manuscript.

Handling Editor: Erwin Dreyer

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Liu, W., Wang, Y., Gong, X. et al. Changes in growth and soil microbial communities in reciprocal grafting clones between Populus deltoides males and females exposed to water deficit conditions. Annals of Forest Science 76, 118 (2019) doi:10.1007/s13595-019-0897-9

Download citation

Keywords

  • Grafting
  • Inorganic nitrogen pool
  • PLFAs
  • Nitrogen cycling