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Plant sciences, sustainable farming systems and food quality
RESEARCH ARTICLE

Improvement of some growth and yield parameters of faba bean (Vicia faba) by inoculation with Rhizobium laguerreae and arbuscular mycorrhizal fungi

Sandra Pereira https://orcid.org/0000-0003-2998-814X A B F , Ângela Mucha A , Berta Gonçalves A C , Eunice Bacelar A C , Aleš Látr D , Helena Ferreira A C , Irene Oliveira A E , Eduardo Rosa A B and Guilhermina Marques A B
+ Author Affiliations
- Author Affiliations

A CITAB – Centre for the Research and Technology of Agro-Environmental and Biological Sciences, University of Trás-os-Montes and Alto Douro, 5001-801 Vila Real, Portugal.

B Department of Agronomy, University of Trás-os-Montes and Alto Douro, 5000-801 Vila Real, Portugal.

C Department of Biology and Environment, University of Trás-os-Montes and Alto Douro, 5000-801 Vila Real, Portugal.

D Symbiom Ltd, Sázava 170, 56301 Lanškroun, Czech Republic.

E CEMAT-IST-UL – Centre for Computational and Stochastic Mathematics, University of Lisbon, 1749-016 Lisbon, Portugal.

F Corresponding author. Email: sirp@utad.pt

Crop and Pasture Science 70(7) 595-605 https://doi.org/10.1071/CP19016
Submitted: 11 January 2019  Accepted: 23 April 2019   Published: 5 August 2019

Abstract

The use of improved biofertilisers such as rhizobia and arbuscular mycorrhizal fungi (AMF) in legume crops is a promising technology that can be an alternative source of nitrogen and phosphorus. A common problem when growing faba bean (Vicia faba L.) and other leguminous plants is the low efficiency of native rhizobial strains. Consequently, there is a need to search for efficient nitrogen-fixing inoculant strains able to increase crop productivity. This study aimed to test the effects of single and dual inoculation with Rhizobium laguerreae and AMF on the growth and yield of faba bean plants. Several parameters were evaluated at flowering stage (number of flowers, stems and leaves, shoot and root biomass, leaf area, leaf mass per area and leaf area ratio, and gas-exchange parameters) and at harvesting stage (number and weight of pods and seeds). Plants receiving single inoculation with Rhizobium laguerreae showed a significant increase in number of leaves, leaf area, leaf mass per area and leaf area ratio, as well as in all yield parameters. Single inoculation with AMF also significantly increased the yield parameters of faba bean plants. Co-inoculation presented significant improvements in leaf area ratio and in all productivity parameters compared with the control, but co-inoculation was not significantly different from the individual inoculations.

Additional keywords: broad bean, tripartite symbiosis.


References

Abd-Alla M, El-Enany A-WE, Nafady NA, Khalaf DM, Morsy FM (2014) Synergistic interaction of Rhizobium leguminosarum bv. viciae and arbuscular mycorrhizal fungi as a plant growth promoting biofertilizers for faba bean (Vicia faba L.) in alkaline soil. Microbiology Research 169, 49–58.
Synergistic interaction of Rhizobium leguminosarum bv. viciae and arbuscular mycorrhizal fungi as a plant growth promoting biofertilizers for faba bean (Vicia faba L.) in alkaline soil.Crossref | GoogleScholarGoogle Scholar |

Abiala MA, Popoola OO, Olawuyi OJ, Oyelude JO, Akanmu AO, Killani AS (2013) Harnessing the potentials of vesicular arbuscular mycorrhizal (VAM) fungi to plant growth—a review. International Journal of Pure and Applied Sciences and Technology 14, 61–79.

Ali A, Choudhry MA, Tanveer A (2000) Response of mung bean (Vigna radiata L.) genotypes to rhizobia culture. Pakistan Journal of Agricultural Sciences 37, 1–2.

Amanullah MJH, Nawab K, Ali A (2007) Response of specific leaf area (SLA), leaf area index (LAI) and leaf area ratio (LAR) of maize (Zea mays L.) to plant density, rate and timing of nitrogen application. World Applied Sciences Journal 2, 235–243.

Bacelar EA, Correia CM, Moutinho-Pereira JM, Gonçalves BC, Lopes JI, Torres-Pereira JMG (2004) Sclerophylly and leaf anatomical traits of five field-grown olive cultivars growing under drought conditions. Tree Physiology 24, 233–239.
Sclerophylly and leaf anatomical traits of five field-grown olive cultivars growing under drought conditions.Crossref | GoogleScholarGoogle Scholar | 14676039PubMed |

Bacelar EA, Santos DL, Moutinho-Pereira JM, Lopes JI, Gonçalves BC, Ferreira TC, Correia CM (2007b) Physiological behaviour, oxidative damage and antioxidative protection of olive trees grown under different irrigation regimes. Plant and Soil 292, 1–12.
Physiological behaviour, oxidative damage and antioxidative protection of olive trees grown under different irrigation regimes.Crossref | GoogleScholarGoogle Scholar |

Bacelar EA, Moutinho-Pereira JM, Gonçalves BC, Lopes JI, Correia CM (2009) Physiological responses of different olive genotypes to drought conditions. Acta Physiologiae Plantarum 31, 611–621.
Physiological responses of different olive genotypes to drought conditions.Crossref | GoogleScholarGoogle Scholar |

Bejandi TK, Sharifii RS, Sedghi M, Namvar A (2011) Effects of plant density, Rhizobium inoculation and microelements on nodulation, chlorophyll content and yield of chickpea (Cicer arietinum L.). Annals of Biological Research 23, 951–958.

Bethlenfalvay GJ, Pacovsky RS, Bayne HG, Stafford AE (1982) Interactions between nitrogen fixation, mycorrhizal colonization, and host-plant growth in the PhaseolusRhizobium–Glomus symbiosis. Plant Physiology 70, 446–450.
Interactions between nitrogen fixation, mycorrhizal colonization, and host-plant growth in the PhaseolusRhizobium–Glomus symbiosis.Crossref | GoogleScholarGoogle Scholar | 16662513PubMed |

Carvalho A, Schmidt L, Santos FD, Delicado A (2014) Climate change research and policy in Portugal. Wiley Interdisciplinary Reviews: Climate Change 5, 199–217.
Climate change research and policy in Portugal.Crossref | GoogleScholarGoogle Scholar |

Crépon K, Marget P, Peyronnet C, Carrouée B, Arese P, Duc G (2010) Nutritional value of faba bean (Vicia faba L.) seeds for feed and food. Field Crops Research 115, 329–339.
Nutritional value of faba bean (Vicia faba L.) seeds for feed and food.Crossref | GoogleScholarGoogle Scholar |

Denton MD, Pearce DJ, Peoples MB (2013) Nitrogen contributions from faba bean (Vicia faba L.) reliant on soil rhizobia or inoculation. Plant and Soil 365, 363–374.
Nitrogen contributions from faba bean (Vicia faba L.) reliant on soil rhizobia or inoculation.Crossref | GoogleScholarGoogle Scholar |

Downton WJS, Loveys BR, Grant WJR (1988) Non-uniform stomatal closure induced by water stress causes putative non-stomatal inhibition of photosynthesis. New Phytologist 110, 503–509.
Non-uniform stomatal closure induced by water stress causes putative non-stomatal inhibition of photosynthesis.Crossref | GoogleScholarGoogle Scholar |

Dubova I, Šenberga A, Alsiņa I (2015) The effect of double inoculation on the broad beans (Vicia faba L.) yield quality. Research for Rural Development 1, 34–39.

FAOSTAT (2018) Statistics Division. Food and Agriculture Organization of the United Nations, Rome. Available at: www.fao.org/faostat/en/#home (accessed 9 April 2018).

Gianinazzi S, Gollotte A, Binet M-N, van Tuinen D, Redecker D, Wipf D (2010) Agroecology: the key role of arbuscular mycorrhizas in ecosystem services. Mycorrhiza 20, 519–530.
Agroecology: the key role of arbuscular mycorrhizas in ecosystem services.Crossref | GoogleScholarGoogle Scholar | 20697748PubMed |

Hardarson G, Atkins C (2003) Optimising biological N2 fixation by legumes in farming systems. Plant and Soil 252, 41–54.
Optimising biological N2 fixation by legumes in farming systems.Crossref | GoogleScholarGoogle Scholar |

Ismaiel AA, Hegazy HS, Azb MA (2014) Physiological response of Vicia faba L. to inoculation with Rhizobium and arbuscular mycorrhizal fungi: Comparative study for irrigation with Nile water and wastewater. AJCS 8, 781–790.

Jensen HL (1942) Nitrogen fixation in leguminous plants. II. Is symbiotic nitrogen fixation influenced by Azotobacter? Proceedings of the Linnean Society of New South Wales 67, 205–212.

Jensen ES, Peoples MB, Nielsen HH (2010) Faba bean in cropping systems. Field Crops Research 115, 203–216.
Faba bean in cropping systems.Crossref | GoogleScholarGoogle Scholar |

Jia YS, Gray VMS, Straker CJ (2004) The influence of Rhizobium and arbuscular mycorrhizal fungi on nitrogen and phosphorus accumulation by Vicia faba. Annals of Botany 94, 251–258.
The influence of Rhizobium and arbuscular mycorrhizal fungi on nitrogen and phosphorus accumulation by Vicia faba.Crossref | GoogleScholarGoogle Scholar |

Jordan DC, Genus I (1984) Rhizobium Frank 1889, 388AL. In ‘Bergey’s manual of systematic bacteriology’. (Eds NR Krieg, JG Holt) pp. 136–139. (Williams and Wilkins: Baltimore, MD, USA)

Kaya C, Ashraf M, Sonmez O, Aydemir S, Tuna AL, Cullu MA (2009) The influence of arbuscular mycorrhizal colonisation on key growth parameters and fruit yield of pepper plants grown at high salinity. Scientia Horticulturae 121, 1–6.
The influence of arbuscular mycorrhizal colonisation on key growth parameters and fruit yield of pepper plants grown at high salinity.Crossref | GoogleScholarGoogle Scholar |

Köpke U, Nemecek T (2010) Ecological services of faba bean. Field Crops Research 115, 217–233.
Ecological services of faba bean.Crossref | GoogleScholarGoogle Scholar |

Ladha JK, Wade L, Dobermann A, Reichardt W, Kirk GJD, Piggin C (1998) Rainfed lowland rice. In ‘Advances in nutrient management research’. (International Rice Research Institute: Manila, The Philippines)

Laguerre G, Nour SM, Macheret V, Sanjuan J, Drouin P, Amarger N (2001) Classification of rhizobia based on nodC and nifH gene analysis reveals a close phylogenetic relationship among Phaseolus vulgaris symbionts. Microbiology 147, 981–993.
Classification of rhizobia based on nodC and nifH gene analysis reveals a close phylogenetic relationship among Phaseolus vulgaris symbionts.Crossref | GoogleScholarGoogle Scholar | 11283294PubMed |

Lalitha S, Santhaguru K (2012) Improving soil physical properties and effect on tree legume seedlings growth under barren soil. Agricultural Science Research Journal 2, 126–130.

Li Y, Liu Z, Hou H, Lei H, Zhu X, Li X, He X, Tian C (2013) Arbuscular mycorrhizal fungi-enhanced resistance against Phytophthora sojae infection on soybean leaves is mediated by a network involving hydrogen peroxide, jasmonic acid, and the metabolism of carbon and nitrogen. Acta Physiologiae Plantarum 35, 3465–3475.
Arbuscular mycorrhizal fungi-enhanced resistance against Phytophthora sojae infection on soybean leaves is mediated by a network involving hydrogen peroxide, jasmonic acid, and the metabolism of carbon and nitrogen.Crossref | GoogleScholarGoogle Scholar |

Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods in Enzymology 148, 350–382.
Chlorophylls and carotenoids: pigments of photosynthetic biomembranes.Crossref | GoogleScholarGoogle Scholar |

Lopez-Iglesias B, Olmo M, Gallardo A, Villar R (2014) Short-term effects of litter from 21 woody species on plant growth and root development. Plant and Soil 381, 177–191.
Short-term effects of litter from 21 woody species on plant growth and root development.Crossref | GoogleScholarGoogle Scholar |

Malik MA, Cheema MA, Khan HZ, Wahid MA (2006) Growth and yield response of soybean to seed inoculation and varying phosphorus. Journal of Agricultural Research 44, 47–53.

McGonigle TP, Miller MH, Evan DG, Faichild GL, Swan JA (1990) A new method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi. New Phytologist 115, 495–501.
A new method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi.Crossref | GoogleScholarGoogle Scholar |

Medrano H, Escalona JM, Bota J, Gulías J, Flexas J (2002) Regulation of photosynthesis of C3 plants in response to progressive drought: stomatal conductance as a reference parameter. Annals of Botany 89, 895–905.
Regulation of photosynthesis of C3 plants in response to progressive drought: stomatal conductance as a reference parameter.Crossref | GoogleScholarGoogle Scholar | 12102515PubMed |

Mei PP, Gui LG, Wang P, Huang JC, Long HY, Christie P, Li L (2012) Maize/faba bean intercropping with rhizobia inoculation enhances productivity and recovery of fertilizer P in a reclaimed desert soil. Field Crops Research 130, 19–27.
Maize/faba bean intercropping with rhizobia inoculation enhances productivity and recovery of fertilizer P in a reclaimed desert soil.Crossref | GoogleScholarGoogle Scholar |

Mohammad MJ, Malkawi HI, Shibli R (2003) Effects of mycorrhizal fungi and phosphorus fertilization on growth and nutrient uptake of barley grown on soils with different levels of salts. Journal of Plant Nutrition 26, 125–137.
Effects of mycorrhizal fungi and phosphorus fertilization on growth and nutrient uptake of barley grown on soils with different levels of salts.Crossref | GoogleScholarGoogle Scholar |

Moutinho-Pereira J, Magalhães N, Gonçalves B, Bacelar E, Brito M, Correia C (2004) Leaf gas exchange and water relations of grapevines grown in three different conditions. Photosynthetica 42, 81–86.
Leaf gas exchange and water relations of grapevines grown in three different conditions.Crossref | GoogleScholarGoogle Scholar |

Moutinho-Pereira JM, Correia CM, Gonçalves B, Bacelar EA, Torres-Pereira JM (2007) Gas exchange and water relations of three Vitis vinifera L. cultivars growing under Mediterranean climate. Photosynthetica 45, 202–207.
Gas exchange and water relations of three Vitis vinifera L. cultivars growing under Mediterranean climate.Crossref | GoogleScholarGoogle Scholar |

Nadeem SM, Ahmad M, Zahir ZA, Javaid A, Ashraf M (2014) The role of mycorrhizae and plant growth promoting rhizobacteria (PGPR) in improving crop productivity under stressful environments. Biotechnology Advances 32, 429–448.
The role of mycorrhizae and plant growth promoting rhizobacteria (PGPR) in improving crop productivity under stressful environments.Crossref | GoogleScholarGoogle Scholar | 24380797PubMed |

Netto AT, Campostrini E, Oliveira JG, Bressan-Smith RE (2005) Photosynthetic pigments, nitrogen, chlorophyll a fluorescence and SPAD-502 readings in coffee leaves. Scientia Horticulturae 104, 199–209.
Photosynthetic pigments, nitrogen, chlorophyll a fluorescence and SPAD-502 readings in coffee leaves.Crossref | GoogleScholarGoogle Scholar |

Oliveira RS, Boyer LR, Carvalho MF, Jeffries P, Vosátka M, Castro PML, Dodd JC (2005) Synergistic effect of Glomus intraradices and Frankia spp. on the growth and stress recovery of Alnus glutinosa in an alkaline anthropogenic sediment. Chemosphere 60, 1462–1470.
Synergistic effect of Glomus intraradices and Frankia spp. on the growth and stress recovery of Alnus glutinosa in an alkaline anthropogenic sediment.Crossref | GoogleScholarGoogle Scholar | 16054916PubMed |

Oliveira RS, Carvalho P, Marques G, Ferreira L, Pereira S, Nunes M, Rocha I, Ma Y, Carvalho MF, Vosátka M, Freitas H (2017) Improved grain yield of cowpea (Vigna unguiculata) under water deficit after inoculation with Bradyrhizobium elkanii and Rhizophagus irregularis. Crop & Pasture Science 68, 1052–1059.
Improved grain yield of cowpea (Vigna unguiculata) under water deficit after inoculation with Bradyrhizobium elkanii and Rhizophagus irregularis.Crossref | GoogleScholarGoogle Scholar |

Omomowo IO, Fadiji AE, Omomowo OI (2018) Assessment of bio-efficacy of Glomus versiforme and Trichoderma harzianum in inhibiting powdery mildew disease and enhancing the growth of cowpea. Annals of Agricultural Science 63, 9–17.
Assessment of bio-efficacy of Glomus versiforme and Trichoderma harzianum in inhibiting powdery mildew disease and enhancing the growth of cowpea.Crossref | GoogleScholarGoogle Scholar |

Oyewole BO, Olawuyi OJ, Odebode AC, Abiala MA (2017) Influence of arbuscular mycorrhiza fungi (AMF) on drought tolerance and charcoal rot disease of cowpea. Biotechnology Reports 14, 8–15.
Influence of arbuscular mycorrhiza fungi (AMF) on drought tolerance and charcoal rot disease of cowpea.Crossref | GoogleScholarGoogle Scholar | 28459003PubMed |

Peoples MB, Herridge DF, Ladha JK (1995) Biological nitrogen fixation: an efficient source of nitrogen for sustainable agricultural production? Plant and Soil 174, 3–28.
Biological nitrogen fixation: an efficient source of nitrogen for sustainable agricultural production?Crossref | GoogleScholarGoogle Scholar |

Poorter H, Niinemets Ü, Poorter L, Wright IJ, Villar R (2009) Causes and consequences of variation in leaf mass per area (LMA): a meta-analysis. New Phytologist 182, 565–588.
Causes and consequences of variation in leaf mass per area (LMA): a meta-analysis.Crossref | GoogleScholarGoogle Scholar | 19434804PubMed |

Pozo M, Verhage A, García-Andrade J, García JM, Azcón-Aguilar C (2009) Priming plant defence against pathogens by arbuscular mycorrhizal fungi. In ‘Mycorrhizas—functional processes and ecological impact’. (Eds C Azcón-Aguilar, J Barea, S Gianinazzi, V Gianinazzi-Pearson) (Springer: Berlin)

Rajasekaran S, Nagarajan SM, Arumugam K, Sravanamuthu R, Balamurugan S (2006) Effect of dual inoculation (AM fungi and Rhizobium) on chlorophyll content of Arachis hypogaea L. CV. TMV-2. Plant Archives 6, 671–672.

Ravikumar R (2012) Growth effects of Rhizobium inoculation in some legume plants. International Journal of Current Science 1–6.

Reich PB (2014) The worldwide ‘fast–slow’ plant economics spectrum: a traits manifesto. Journal of Ecology 102, 275–301.
The worldwide ‘fast–slow’ plant economics spectrum: a traits manifesto.Crossref | GoogleScholarGoogle Scholar |

Ribet J, Drevon JJ (1996) The phosphorus requirement of N2-fixing and urea-fed Acacia mangium. New Phytologist 132, 383–390.
The phosphorus requirement of N2-fixing and urea-fed Acacia mangium.Crossref | GoogleScholarGoogle Scholar | 26763634PubMed |

Rodelas B, Gonzalez-Lopez J, Pozo C, Salmeron V, Martinez-Toledo MV (1999) Response of faba bean (Vicia faba L.) to combined inoculation with Azotobacter and Rhizobium leguminosarum bv. viceae. Applied Soil Ecology 12, 51–59.
Response of faba bean (Vicia faba L.) to combined inoculation with Azotobacter and Rhizobium leguminosarum bv. viceae.Crossref | GoogleScholarGoogle Scholar |

Rogel MA, Ormeno-Orrillo E, Romero EM (2011) Symbiovars in rhizobia reflect bacterial adaptation to legumes. Systematic and Applied Microbiology 34, 96–104.
Symbiovars in rhizobia reflect bacterial adaptation to legumes.Crossref | GoogleScholarGoogle Scholar | 21306854PubMed |

Saidi S, Ramírez-Bahena MH, Santillana N, Zúñiga D, Álvarez-Martínez E, Peix A, Mhamdi R, Velázquez E (2013) Rhizobium laguerreae sp. nov. nodulates Vicia faba on several continents. International Journal of Systematic and Evolutionary Microbiology 64, 242–247.

Scheublin TR, van der Heijden MGA (2006) Arbuscular mycorrhizal fungi colonize nonfixing root nodules of several legume species. New Phytologist 172, 732–738.
Arbuscular mycorrhizal fungi colonize nonfixing root nodules of several legume species.Crossref | GoogleScholarGoogle Scholar | 17096798PubMed |

Schimel JP, Bennett J (2004) Nitrogen mineralization: challenges of a changing paradigm. Ecology 85, 591–602.
Nitrogen mineralization: challenges of a changing paradigm.Crossref | GoogleScholarGoogle Scholar |

Schultz HR (1996) Leaf absorptance of visible radiation in Vitis vinifera L.: estimates of age and shade effects with a simple field method. Scientia Horticulturae 66, 93–102.
Leaf absorptance of visible radiation in Vitis vinifera L.: estimates of age and shade effects with a simple field method.Crossref | GoogleScholarGoogle Scholar |

Sesták Z (1971) Determination of chlorophylls a and b. In ‘Plant photosynthetic production. Manual of methods’. (Eds Z Sesták, J Catský, PG Jarvis) pp. 672–702. (Dr W Junk NV Publishers: The Hague)

Sharma L, Gonçalves F, Oliveira I, Torres L, Marques G (2018a) Insect-associated fungi from naturally mycosed vine mealybug Planococcus ficus (Signoret) (Hemiptera: Pseudococcidae). Biocontrol Science and Technology 28, 122–141.
Insect-associated fungi from naturally mycosed vine mealybug Planococcus ficus (Signoret) (Hemiptera: Pseudococcidae).Crossref | GoogleScholarGoogle Scholar |

Sharma L, Oliveira I, Torres L, Marques G (2018b) Entomopathogenic fungi in Portuguese vineyards soils: suggesting a ‘Galleria–Tenebrio-bait method’ as bait-insects Galleria and Tenebrio significantly underestimate the respective recoveries of Metarhizium (robertsii) and Beauveria (bassiana). MycoKeys 38, 1–23.
Entomopathogenic fungi in Portuguese vineyards soils: suggesting a ‘Galleria–Tenebrio-bait method’ as bait-insects Galleria and Tenebrio significantly underestimate the respective recoveries of Metarhizium (robertsii) and Beauveria (bassiana).Crossref | GoogleScholarGoogle Scholar |

Sheng M, Tang M, Chen H, Yang BW, Zhang FF, Huang YH (2009) Influence of arbuscular mycorrhizae on the root system of maize plants under salt stress. Canadian Journal of Microbiology 55, 879–886.
Influence of arbuscular mycorrhizae on the root system of maize plants under salt stress.Crossref | GoogleScholarGoogle Scholar | 19767861PubMed |

Sivaprasad P, Rai PV (1987) Mechanism of enhanced nodulation in vesicular arbuscular mycorrhizal (VAM) pigeon pea, Cajanus cajan (L.) Millsp. Agricultural Research Journal of Kerala 25, 99–102.

Smith SE, Read DJ (2008) ‘Mycorrhizal symbiosis.’ (Academic Press: Amsterdam)

Tian CF, Wang ET, Han TX, Sui XH, Chen WX (2007) Genetic diversity of rhizobia associated with Vicia faba in three ecological regions of China. Archives of Microbiology 188, 273–282.
Genetic diversity of rhizobia associated with Vicia faba in three ecological regions of China.Crossref | GoogleScholarGoogle Scholar | 17479251PubMed |

Van Berkum P, Beyene D, Vera FT, Keyser HH (1995) Variability among Rhizobium strains originating from nodules of Vicia faba. Applied and Environmental Microbiology 61, 2649–2653.

Vierheilig H, Coughlan AP, Wyss U, Piche Y (1998) Ink and vinegar, a simple staining technique for arbuscular-mycorrhizal fungi. Applied and Environmental Microbiology 64, 5004–5007.

von Caemmerer S, Farquhar GD (1981) Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 153, 376–387.
Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves.Crossref | GoogleScholarGoogle Scholar | 24276943PubMed |

Witkowski ETF, Lamont BB (1991) Leaf specific mass confounds leaf density and thickness. Oecologia 88, 486–493.
Leaf specific mass confounds leaf density and thickness.Crossref | GoogleScholarGoogle Scholar |

Xie ZP, Staehelin C, Vierheilig H, Wiemken A, Jabbouri S, Broughton WJ, Vogeli-Lange R, Boller T (1995) Rhizobial nodulation factors stimulate mycorrhizal colonization of nodulating and nonnodulating soybeans. Plant Physiology 108, 1519–1525.
Rhizobial nodulation factors stimulate mycorrhizal colonization of nodulating and nonnodulating soybeans.Crossref | GoogleScholarGoogle Scholar | 12228558PubMed |

Xu KW, Zou L, Penttinen P, Wang K, Heng NN, Zhang XP, Chen Q, Zhao K, Chen YX (2015) Symbiotic effectiveness and phylogeny of rhizobia isolated from faba bean (Vicia faba L.) in Sichuan hilly areas, China. Systematic and Applied Microbiology 38, 515–523.
Symbiotic effectiveness and phylogeny of rhizobia isolated from faba bean (Vicia faba L.) in Sichuan hilly areas, China.Crossref | GoogleScholarGoogle Scholar | 26242694PubMed |

Youseif SH, El-Megeed FHA, Ageez A, Cocking EC, Saleh SA (2014) Phylogenetic multilocus sequence analysis of native rhizobia nodulating faba bean (Vicia faba L.) in Egypt. Systematic and Applied Microbiology 37, 560–569.
Phylogenetic multilocus sequence analysis of native rhizobia nodulating faba bean (Vicia faba L.) in Egypt.Crossref | GoogleScholarGoogle Scholar | 25458609PubMed |

Youseif SH, El-Megeed FHA, Saleh SA (2017) Improvement of faba bean yield using Rhizobium/Agrobacterium inoculant in low-fertility sandy soil. Agronomy 7, 1–12.

Zohary D, Hopf M (2000) ‘Domestication of plants in the Old World.’ 3rd edn. (Oxford University Press: Oxford, UK)