Does mycorrhizal colonisation vary between maize and sunflower under limitations to radiation source or carbohydrate sink?
Fernanda Covacevich A B E , Julieta Martínez Verneri B and Guillermo A. A. Dosio B C D EA Instituto de Investigaciones en Biodiversidad y Biotecnología – Fundación para Investigaciones Biológicas Aplicadas, Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Mar del Plata, Argentina.
B Unidad Integrada Balcarce (Estación Experimental Agropecuaria INTA/Facultad de Ciencias Agrarias, Universidad Nacional de Mar del Plata), Ruta 226 Km 73.5 (7620), Balcarce, Argentina.
C Laboratorio de Fisiología Vegetal, Facultad de Ciencias Agrarias, Universidad Nacional de Mar del Plata, Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Balcarce, Argentina.
D Corresponding author. Email: gdosio@mdp.edu.ar
E These authors contributed equally to the paper.
Crop and Pasture Science 69(10) 974-984 https://doi.org/10.1071/CP17340
Submitted: 15 September 2017 Accepted: 30 August 2018 Published: 4 October 2018
Abstract
The aim of this work was to analyse and compare indigenous arbuscular mycorrhizal colonisation (AMC) in relation to growth and total soluble carbohydrates (TSC) in two major, physiologically contrasting crop species: maize (Zea mays L.) and sunflower (Helianthus annuus L.). In order to promote contrasting TSC concentrations, we modified the radiation source by shading and the carbohydrate sink by manipulating reproductive sinks at different phenological stages during the grain-filling period in two field experiments. We assessed plant dry matter, TSC in stems, and root AMC from flowering until final harvest. AMC during the grain-filling period decreased in maize and increased in sunflower. A sink limitation increased AMC in maize, and reduced it in sunflower. A source limitation decreased AMC in both species, especially in sunflower. AMC was positively related to TSC in maize, but negatively in sunflower. The relationship was affected by shading in sunflower, but not in maize. In both species, a different linear model described the relationship between AMC and TSC in plants submitted to the removal of the reproductive organs. The results highlight the role of carbohydrates in mediating mycorrhizal formation, and show for the first time the opposite AMC–TSC relationships in maize and sunflower.
Additional keywords: agronomy, annual crops, endophytes, plant–microbe interactions, soil fungi, soluble carbohydrates, symbiosis.
References
Allison JC, Weinmann H (1970) Effect of absence of developing grain on carbohydrate content and senescence of maize leaves. Plant Physiology 46, 435–436.| Effect of absence of developing grain on carbohydrate content and senescence of maize leaves.Crossref | GoogleScholarGoogle Scholar |
Andrade FH, Ferreiro MA (1996) Reproductive growth of maize, sunflower and soybean at different source levels during grain filling. Field Crops Research 48, 155–165.
| Reproductive growth of maize, sunflower and soybean at different source levels during grain filling.Crossref | GoogleScholarGoogle Scholar |
Astiz Imaz P, Barbieri PA, Echeverría HE, Sainz Rozas HR, Covacevich F (2014) Indigenous mycorrhizal fungi from Argentina increase Zn nutrition of maize modulated by Zn fertilization. Soil & Environment 31, 23–32.
Bago B, Pfeffer PE, Shachar-Hill Y (2000) Carbon metabolism and transport in arbuscular mycorrhizas. Plant Physiology 124, 949–957.
| Carbon metabolism and transport in arbuscular mycorrhizas.Crossref | GoogleScholarGoogle Scholar |
Barbieri PA, Sainz Rozas HR, Covacevich F, Echeverría HE (2014) Phosphorus placement effects on phosphorous recovery efficiency and grain yield of wheat under no-tillage in the humid Pampas of Argentina. International Journal of Agronomy 507105
Barea J, Azcon-Aguilar C (1983) Mycorrhizas and their significance in nodulating nitrogen fixing plants. Advances in Agronomy 36, 1–54.
| Mycorrhizas and their significance in nodulating nitrogen fixing plants.Crossref | GoogleScholarGoogle Scholar |
Bethlenfalvay GJ, Pacovsky RS (1983) Light effects in mycorrhizal soybeans. Plant Physiology 73, 969–972.
| Light effects in mycorrhizal soybeans.Crossref | GoogleScholarGoogle Scholar |
Bryla DR, Eissenstat DM (2005) Respiratory costs of mycorrhizal associations. In ‘Advances in photosynthesis and respiration’. (Eds H Lambers, M Ribas-Carbo) pp. 207–224. (Springer: Dordrecht, The Netherlands)
Chalk P, Souza R, Urquiaga S, Alves B, Boddey R (2006) The role of arbuscular mycorrhiza in legume symbiotic performance. Soil Biology & Biochemistry 38, 2944–2951.
| The role of arbuscular mycorrhiza in legume symbiotic performance.Crossref | GoogleScholarGoogle Scholar |
Daft M, El-Giahmi A (1978) Effect of arbuscular mycorrhiza on plant growth. VIII. Effects of defoliation and light on selected hosts. New Phytologist 80, 365–372.
| Effect of arbuscular mycorrhiza on plant growth. VIII. Effects of defoliation and light on selected hosts.Crossref | GoogleScholarGoogle Scholar |
Di Rienzo JA, Casanoves F, Balzarini MG, Gonzalez L, Tablada M, Robledo CW (2016) InfoStat. Grupo InfoStat, FCA, Universidad Nacional de Córdoba, Argentina. Available at: http://www.infostat.com.ar (accessed May–December 2016).
DuBois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Analytical Chemistry 28, 350–356.
| Colorimetric method for determination of sugars and related substances.Crossref | GoogleScholarGoogle Scholar |
Echeverría HE, García FO (2015) ‘Fertilidad de suelos y fertilización de cultivos.’ (INTA, IPNI: Buenos Aires)
Fernandez M, Gutierrez Boem FH, Rubio G (2009) Arbuscular mycorrhizal colonization and mycorrhizal dependency: a comparison among soybean, sunflower and maize. In ‘Proceedings International Plant Nutrition Colloquium XVI’. UC Davis, Sacramento, CA. Available at: http://escholarship.org/uc/item/0vd8n24g (accessed January 2017)
Gan S, Amasino RM (1997) Molecular genetic regulation and manipulation of leaf senescence. Plant Physiology 113, 313–319.
| Molecular genetic regulation and manipulation of leaf senescence.Crossref | GoogleScholarGoogle Scholar |
Gosling P, Mead A, Proctor M, Hammond JP, Bending GD (2013) Contrasting arbuscular mycorrhizal communities colonizing different host plants show a similar response to a soil phosphorus concentration gradient. New Phytologist 198, 546–556.
| Contrasting arbuscular mycorrhizal communities colonizing different host plants show a similar response to a soil phosphorus concentration gradient.Crossref | GoogleScholarGoogle Scholar |
Gowik U, Westhoff P (2011) The path from C3 to C4 photosynthesis. Plant Physiology 155, 56–63.
| The path from C3 to C4 photosynthesis.Crossref | GoogleScholarGoogle Scholar |
Hall AJ, Connor DJ, Whitfield DM (1989) Contribution of pre-anthesis assimilates to grain-filling in irrigated and water-stressed sunflower crops. I. Estimates using labeled carbon. Field Crops Research 20, 95–112.
| Contribution of pre-anthesis assimilates to grain-filling in irrigated and water-stressed sunflower crops. I. Estimates using labeled carbon.Crossref | GoogleScholarGoogle Scholar |
Hazard C, Gosling P, van der Gast C, Mitchell DT, Doohan FM, Bending GD (2013) The role of local environment and geographical distance in determining community composition of arbuscular mycorrhizal fungi at the landscape scale. The ISME Journal 7, 498–508.
| The role of local environment and geographical distance in determining community composition of arbuscular mycorrhizal fungi at the landscape scale.Crossref | GoogleScholarGoogle Scholar |
Ho I, Below FE, Hageman RH (1987) Effect of head removal on leaf senescence of sunflower. Plant Physiology 83, 844–848.
| Effect of head removal on leaf senescence of sunflower.Crossref | GoogleScholarGoogle Scholar |
Johnson NC, Graham JH, Smith FA (1997) Functioning of mycorrhizal associations along the mutualism-parasitism continuum. New Phytologist 135, 575–585.
| Functioning of mycorrhizal associations along the mutualism-parasitism continuum.Crossref | GoogleScholarGoogle Scholar |
Kiers ET, Duhamel M, Beesetty Y, Mensah JA, Franken O, Verbruggen E, Fellbaum CR, Kowalchuk GA, Hart MM, Bago A, Palmer TM, West SA, Vandenkoornhuyse P, Jansa J, Bücking H (2011) Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333, 880–882.
| Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis.Crossref | GoogleScholarGoogle Scholar |
Konvalinková T, Jansa J (2016) Lights off for arbuscular mycorrhiza: on its symbiotic functioning under light deprivation. Frontiers of Plant Science 7, 782
| Lights off for arbuscular mycorrhiza: on its symbiotic functioning under light deprivation.Crossref | GoogleScholarGoogle Scholar |
Konvalinková T, Püschel D, Janoušková M, Gryndler M, Jansa J (2015) Duration and intensity of shade differentially affects mycorrhizal growth-and phosphorus uptake responses of Medicago truncatula. Frontiers of Plant Science 6, 1–6.
Li HY, Zhu YG, Marschner P, Smith FA, Smith SE (2005) Wheat responses to arbuscular mycorrhizal fungi in a highly calcareous soil differ from those of clover, and change with plant development and P supply. Plant and Soil 277, 221–232.
| Wheat responses to arbuscular mycorrhizal fungi in a highly calcareous soil differ from those of clover, and change with plant development and P supply.Crossref | GoogleScholarGoogle Scholar |
Lindoo SJ, Nooden LD (1977) Studies on the behavior of the senescence signal in Anoka soybeans. Plant Physiology 59, 1136–1140.
| Studies on the behavior of the senescence signal in Anoka soybeans.Crossref | GoogleScholarGoogle Scholar |
Liu A, Hamel C, Elmi AA, Zhang T, Smith DL (2003) Reduction of the available phosphorus pool in field soils growing maize genotypes with extensive mycorrhizal development. Canadian Journal of Plant Science 83, 737–744.
| Reduction of the available phosphorus pool in field soils growing maize genotypes with extensive mycorrhizal development.Crossref | GoogleScholarGoogle Scholar |
McGonigle TP, Miller MH, Young D (1999) Mycorrhizae, crop growth, and crop phosphorus nutrition in maize-soybean rotations given various tillage treatments. Plant and Soil 210, 33–42.
| Mycorrhizae, crop growth, and crop phosphorus nutrition in maize-soybean rotations given various tillage treatments.Crossref | GoogleScholarGoogle Scholar |
van der Heijden MGA, Martin FM, Selosse MA, Sanders IR (2015) Mycorrhizal ecology and evolution: the past, the present, and the future. New Phytologist 205, 1406–1423.
Ocampo JA, Azcon R (1985) Relationship between the concentration of sugars in the roots and VA mycorrhizal infection. Plant and Soil 86, 95–100.
| Relationship between the concentration of sugars in the roots and VA mycorrhizal infection.Crossref | GoogleScholarGoogle Scholar |
Olsson PA, Rahm J, Aliasgharzad N (2010) Carbon dynamics in mycorrhizal symbioses is linked to carbon costs and phosphorus benefits. FEMS Microbiology Ecology 72, 125–131.
| Carbon dynamics in mycorrhizal symbioses is linked to carbon costs and phosphorus benefits.Crossref | GoogleScholarGoogle Scholar |
Ortas I (2012) The effect of mycorrhizal fungal inoculation on plant yield, nutrient uptake and inoculation effectiveness under long-term field conditions. Field Crops Research 125, 35–48.
| The effect of mycorrhizal fungal inoculation on plant yield, nutrient uptake and inoculation effectiveness under long-term field conditions.Crossref | GoogleScholarGoogle Scholar |
Peng S, Eissenstat DM, Graham JH, Williams K, Hodge NC (1993) Growth depression in mycorrhizal citrus at high-phosphorus supply: analysis of carbon costs. Plant Physiology 101, 1063–1071.
| Growth depression in mycorrhizal citrus at high-phosphorus supply: analysis of carbon costs.Crossref | GoogleScholarGoogle Scholar |
Phillips J, Hayman D (1970) Procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Transactions of the British Mycological Society 55, 158–161.
| Procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection.Crossref | GoogleScholarGoogle Scholar |
Rajcan I, Tollenaar M (1999) Source:sink ratio and leaf senescence in maize: II. Nitrogen metabolism during grain filling. Field Crops Research 60, 255–265.
| Source:sink ratio and leaf senescence in maize: II. Nitrogen metabolism during grain filling.Crossref | GoogleScholarGoogle Scholar |
Ritchie SW, Hanway JJ, Benson GO (1986) How a corn plant develops. Special Report No. 48, 21. Iowa State University of Science and Technology. Cooperative Extension Services. Ames, Iowa. Available at: http://publications.iowa.gov/id/eprint/18027
Sadras VO, Echarte L, Andrade FH (2000) Profiles of leaf senescence during reproductive growth of sunflower and maize. Annals of Botany 85, 187–195.
| Profiles of leaf senescence during reproductive growth of sunflower and maize.Crossref | GoogleScholarGoogle Scholar |
Same BI, Robson AD, Abbot LK (1983) Phosphorus, soluble carbohydrates and endomycorrhizal infection. Soil Biology & Biochemistry 15, 593–597.
| Phosphorus, soluble carbohydrates and endomycorrhizal infection.Crossref | GoogleScholarGoogle Scholar |
Scheublin T, Ridgway K (2004) Non legumes, legumes, and root nodules harbor different arbuscular mycorrhizal fungal communities. Applied and Environmental Microbiology 70, 6240–6246.
| Non legumes, legumes, and root nodules harbor different arbuscular mycorrhizal fungal communities.Crossref | GoogleScholarGoogle Scholar |
Schmitt A, Pausch J, Kuzyakov Y (2013) C and N allocation in soil under ryegrass and alfalfa estimated by 13C and 15N labeling. Plant and Soil 368, 581–590.
| C and N allocation in soil under ryegrass and alfalfa estimated by 13C and 15N labeling.Crossref | GoogleScholarGoogle Scholar |
Schneiter AA, Miller JF (1981) Description of sunflower growth stages. Crop Science 21, 901–903.
| Description of sunflower growth stages.Crossref | GoogleScholarGoogle Scholar |
Setter TL, Flannigan BA (1986) Sugar and starch redistribution in maize in response to shade and ear temperature treatment. Crop Science 26, 575–579.
| Sugar and starch redistribution in maize in response to shade and ear temperature treatment.Crossref | GoogleScholarGoogle Scholar |
Smith S, Read D (2008) ‘Mycorrhizal symbiosis.’ (Academic Press: Cambridge, UK)
Soil Survey Staff (2014) ‘Keys to Soil Taxonomy.’ 12th edn (USDA-Natural Resources Conservation Service: Washington, DC)
Tahat MM, Sijam K (2012) Mycorrhizal fungi and abiotic environmental conditions relationship. Research Journal of Environmental Sciences 6, 125–133.
| Mycorrhizal fungi and abiotic environmental conditions relationship.Crossref | GoogleScholarGoogle Scholar |
Tester M, Smith SE, Smith FA, Walkers NA (1986) Effects of photon irradiance on the growth of shoots and roots, on the rate of initiation of mycorrhizal infection and on the growth of infection units in Trifolium subterraneum l. New Phytologist 103, 375–390.
| Effects of photon irradiance on the growth of shoots and roots, on the rate of initiation of mycorrhizal infection and on the growth of infection units in Trifolium subterraneum l.Crossref | GoogleScholarGoogle Scholar |
Thomas H, Smart CM (1993) Crops that stay green. Annals of Applied Biology 123, 193–219.
| Crops that stay green.Crossref | GoogleScholarGoogle Scholar |
Thomas H, Stoddart JL (1980) Leaf senescence. Annual Review of Plant Physiology 31, 83–111.
| Leaf senescence.Crossref | GoogleScholarGoogle Scholar |
Thougnon Islas AJ, Hernandez Guijarro K, Eyherabide M, Sainz Rozas HR, Echeverría HE, Covacevich F (2016) Can soil properties and agricultural land use affect arbuscular mycorrhizal fungal communities indigenous from the Argentinean Pampas soils? Applied Soil Ecology 101, 47–56.
| Can soil properties and agricultural land use affect arbuscular mycorrhizal fungal communities indigenous from the Argentinean Pampas soils?Crossref | GoogleScholarGoogle Scholar |
Trouvelot A, Kough JL, Gianinazzi-Pearson V (1986) Mesure du taux de mycorrhization VA d’un système radiculaire. Recherche de methods d’estimation ayent une signification fonctionelle. In ‘Physiological and genetical aspects of mycorrhizae’. (Eds V Gianinazzi-Pearson, S Gianinazzi) pp. 626–630. (INRA: Paris)
Uibopuu A, Moora M, Saks U, Daniell T, Zobel M, Opik M (2009) Differential effect of arbuscular mycorrhizal fungal communities from ecosystems along management gradient on the growth of forest under story plant species. Soil Biology & Biochemistry 41, 2141–2146.
| Differential effect of arbuscular mycorrhizal fungal communities from ecosystems along management gradient on the growth of forest under story plant species.Crossref | GoogleScholarGoogle Scholar |
Walder F, van der Heijden MGA (2015) Regulation of resource exchange in the arbuscular mycorrhizal symbiosis. Nature Plants 1, 15159
| Regulation of resource exchange in the arbuscular mycorrhizal symbiosis.Crossref | GoogleScholarGoogle Scholar |
Wingler A, Purdy S, Mac Lean JA, Pourtau N (2006) The role of sugars in integrating environmental signals during the regulation of leaf senescence. Journal of Experimental Botany 57, 391–399.
| The role of sugars in integrating environmental signals during the regulation of leaf senescence.Crossref | GoogleScholarGoogle Scholar |
Yoshida S (2003) Molecular regulation of leaf senescence. Current Opinion in Plant Biology 6, 79–84.
| Molecular regulation of leaf senescence.Crossref | GoogleScholarGoogle Scholar |