Can functional hologenomics aid tackling current challenges in plant breeding?

Briefings in Functional Genomics

Volumn 15, Issue 4, 2016, Pages 288-297

  Nogales, Amaia ^a   Nobre, Tânia ^a   Valadas, Vera ^a   Ragonezi, Carla ^a,d   Döring, Matthias ^b   Polidoros, Alexios ^c   Arnholdt Schmitt, Birgit ^a  

^a UNIVERSITY OF ÉVORA   (Portugal)

^b SME INOQ GmbH   (Germany)

^c ARISTOTLE UNIVERSITY OF THESSALONIKI   (Greece)

^d UNIVERSIDADE FEDERAL DOS VALES DO JEQUITINHONHA E MUCURI   (Brazil)

Author keywords

Endophytes; Genetic variability; Holobiont; Molecular markers; Phenotype; Plant functionality

Indexed keywords

ATTENTION; ENDOPHYTE; GENETIC VARIABILITY; MICROORGANISM; PHENOTYPE; PLANT BREEDING; SCREENING; GENETICS; GENOMICS; PLANT; PROCEDURES; QUANTITATIVE TRAIT LOCUS;

GENOMICS; PHENOTYPE; PLANT BREEDING; PLANTS; QUANTITATIVE TRAIT LOCI;

EID: 84980050610     PISSN: 20412649     EISSN: 20412657     Source Type: Journal    
DOI: 10.1093/bfgp/elv030     Document Type: Article

References (133)

1. Bilder RM, Sabb FW, Cannon TD, et al. Phenomics: the systematic study of phenotypes on a genome-wide scale. Neuroscience 2009;164(1):30-42.
2. van der Heijden MGA, Bardgett RD, van Straalen NM. The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 2008;11:296-310.
3. Arnholdt-Schmitt B, Valadas V, Döring M. Functional marker development is challenged by the ubiquity of endophytes-a practical perspective. Brief Funct Genom 2016;15:16-21.
4. Rosenberg E, Sharon G, Zilber-Rosenberg I. The hologenome theory of evolution contains Lamarckian aspects within a Darwinian framework. Environ Microbiol 2009;11(12):2959-62.
5. Bosch CGT, McFall-Ngaib, Margaret J. Metaorganisms as the new frontier. Zool 2011;114:185-90.
6. Booth A. Symbiosis, selection, and individuality. Biol Phil 2014;29(5):657-73.
7. Vandenkoornhuyse P, Quaiser A, Duhamel M, et al. The importance of the microbiome of the plant holobiont. New Phytol 2015;206(4):1196-206.
8. Reinhold-Hurek B, Hurek T. Living inside plants: bacterial endophytes. Curr Opin Plant Biol 2011;14:435-43.
9. Gilbert SF, Sapp J, Tauber AI. A symbiotic view of life: we have never been individuals. Q Rev Biol 2012;87(4):325-41.
10. Berg G, Grube M, Schloter M, et al. Unraveling the plant microbiome: looking back and future perspectives. Front Microbiol 2014;5:148.
11. Hurek T. Constraints for endophytic bacteria. In: Sattelmacher B, Horst WJ (eds). The Apoplast of Higher Plants: Compartment of Storage, Transport and Reactions. Dordrecht, Netherlands: Springer, 2007, 395-403.
12. Fisher PJ, Petrini O, Sutton BC. A comparative study of fungal endophytes in leaves, xylem and bark of Eucalyptus in Australia and England. Sydowia 1993;45:338-45.
13. Pirttila AM, Laukkanen H, Pospiech H, et al. Detection of intracellular bacteria in the buds of Scotch pine (Pinus sylvestris L.) by in situ hybridization. Appl Environ Microbiol 2000;66(7):3073-77.
14. Thomas P, Sekhar AC. Live cell imaging reveals extensive intracellular cytoplasmic colonization of banana by normally non-cultivable endophytic bacteria. AoB Plants 2014;plu002. doi: 10.1093/aobpla/plu002.
15. White JF, Jr, Torres MS, Somu MP, et al. Hydrogen peroxide staining to visualize intracellular bacterial infections of seedling root cells. Microsc Res Tech 2014;77(8):566-73.
16. Wilson D. Endophyte-the evolution of a term, and clarification of its use and definition. Oikos 1995;73:274-6.
17. Bacon CW, White JF. Microbial Endophytes. New York, NY: Marcel Dekker Inc., 2000.
18. Hardoim PR, van Overbeek LS, van Elsas JD. Properties of bacterial endophytes and their proposed role in plant growth. Trends Microbiol 2008;16(10):463-71.
19. Rosenberg E, Koren O, Reshef L, et al. The role of microorganisms in coral health, disease and evolution. Nat Rev Microbiol 2007;5:355-62.
20. Saikkonen K, Wäli P, Helander M, et al. Evolution of endophyte-plant symbioses. Trends Plant Sci 2004;9:1360-85.
21. Schardl CL, Leuchtmann A, Spiering MJ. Symbioses of grasses with seedborne fungal endophytes. Annu Rev Plant Biol 2004;55:315-40.
22. Douglas AE. Host benefit and the evolution of specialization in symbiosis. Heredity 1998;81:599-603.
23. Rodriguez RJ, White JF, Arnold AE, et al. Fungal endophytes: diversity and functional roles. New Phytol 2009;182:314-30.
24. Gao FK, Dai CC, Liu XZ. Mechanisms of fungal endophytes in plant protection against pathogens. Afric J Microbiol Res 2010;4:1346-51.
25. Jaber LR, Vidal S. Fungal endophyte negative effects on herbivory are enhanced on intact plants and maintained in a subsequent generation. Ecol Entomol 2010;35:25-36.
26. Gange AC, Eschen R, Wearn JA, et al. Differential effects of foliar endophytic fungi on insect herbivores attacking a herbaceous plant. Oecologia 2012;168:1023-31.
27. Sturz AV, Christie BR, Nowak J. Bacterial endophytes: potential role in developing sustainable systems of crop production. Crit Rev Plant Sci 2000;19(1):1-30.
28. Rodriguez RJ, Henson J, Van Volkenburgh E, et al. Stress tolerance in plants via habitat-adapted symbiosis. ISME J 2008;2:404-16.
29. Rodriguez RJ, Freeman DC, McArthur ED, et al. Symbiotic regulation of plant growth, development and reproduction. Commun Integr Biol 2009;2(2):141-3.
30. Friesen ML, Porter SS, Stark SC, et al. Microbially mediated plant functional traits. Annu Rev Ecol Evol Syst 2011;42:23-46.
31. Duhamel M, Vandenkoornhuyse P. Sustainable agriculture: possible trajectories from mutualistic symbiosis and plant neodomestication. Trends Plant Sci 2013;18:597-600.
32. Goh C-H, Veliz Vallejos DF, Nicotra AB, et al. The impact of beneficial plant-associated microbes on plant phenotypic plasticity. J Chem Ecol 2013;39(7): 826-39.
33. Panke-Buisse K, Poole AC, Goodrich JK, et al. Selection on soil microbiomes reveals reproducible impacts on plant function. ISME J 2015;9:980-9.
34. Wagner MR, Lundberg DS, Coleman-Derr D, et al. Natural soil microbes alter flowering phenology and the intensity of selection on flowering time in a wild Arabidopsis relative. Ecol Lett 2014;17:717-26.
35. Arnold AE, Mejia LC, Kyllo D, et al. Fungal endophytes limit pathogen damage in a tropical tree. Proc Natl Acad Sci USA 2003;100:15649-54.
36. Waller F, Achatz B, Baltruschat H, et al. The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield. PNAS 2005;102:13386-91.
37. Partida-Martinez LP, Heil M. The microbe-free plant: fact or artifact? Front plant Sci 2011;2:100.
38. Ali B, Sabri AN, Ljung K, et al. Auxin production by plant associated bacteria: Impact on endogenous IAA content and growth of Triticum aestivum L. Lett Appl Microbiol 2009;48(5):542-47.
39. Redman RS, Sheehan KB, Stout RG, et al. Thermotolerance conferred to plant host and fungal endophyte during mutualistic symbiosis. Science 2002;298(5598):1581.
40. Castiglioni P, Warner D, Bensen RJ, et al. Bacterial RNA chaperones confer abiotic stress tolerance in plants and improved grain yield in maize under water-limited conditions. Plant Physiol 2008;147(2):446-55.
41. Baltruschat H, Fodor J, Harrach BD, et al. Salt tolerance of barley induced by the root endophyte Piriformospora indica is associated with a strong increase in antioxidants. New Phytol 2008;180:501-10.
42. Zhang H, Kim MS, Sun Y, et al. Soil bacteria confer plant salt tolerance by tissue-specific regulation of the sodium transporter HKT1. Mol Plant Microbe Interact 2008;21(6):737-44.
43. Lugtenberg B, Kamilova F. Plant-growth promoting rhizobacteria. Annu Rev Microbiol 2009;63:541-56.
44. Yang J, Kloepper JW, Ryu CM. Rhizosphere bacteria help plants tolerate abiotic stress. Trends Plant Sci 2009;14:1-4.
45. Margulis L, Fester R. Symbiosis as a source of evolutionary innovation: speciation and morphogenesis. In: Margulis L, Fester R (eds). Cambridge: MIT Press, 1991.
46. Zilber-Rosenberg I, Rosenberg E. Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. FEMS Microbiol Lett 2008;32:723-35.
47. Rosenberg E, Zilberg-Rosenberg I. Symbiosis and development: the hologenome concept. Birth Defects Res 2011;93:56-66.
48. Soen Y. Environmental disruption of host-microbe coadaptation as a potential driving force in evolution. Front Genet 2014;5:168.
49. Panaccione DG, Johnson RD, Wang J, et al. Elimination of ergovaline from grass-Neotyphodium endophyte symbiosis by genetic modification of the endophyte. Proc Natl Sci USA 2001;98:12820-25.
50. Bouton JH, Latch GCM, Hill NS, et al. Reinfection of tall fescue cultivars with non-ergot alkaloid-producing endophytes. Agron J 2002;94:567-74.
51. Woodfield DR, Easton HS. Advances in pasture breeding for animal productivity and health. N Z Vet J 2004;52:300-10.
52. Porras-Alfaro A, Bayman P. Hidden fungi, emergent properties: endophytes and microbiomes. Annu Rev Phytopathol 2011;49:291-315.
53. Guttman D, McHardy AC, Schulze-Lefert P. Microbial genome-enabled insights into plant-microorganism interactions. Nat Rev Genet 2014;15(12):797-813.
54. Rensink WA, Buell CR. Microarray expression profiling resources for plant genomics. Trends Plant Sci 2005;10(12):603-9.
55. Varshney RK, Tuberosa R. Genomics-Assisted Crop Improvement, Vol. 1: Genomics Approaches and Platforms. New York, NY: Springer, 2007.
56. Varshney RK, Tuberosa R. Genomics-Assisted Crop Improvement, Vol. 2: Genomics Applications in Crops. New York, NY: Springer, 2007.
57. Tester M, Langridge P. Breeding technologies to increase crop production in a changingworld. Science 2010;327:818-922.
58. Lorenz AJ, Chao S, Asoro FG, et al. Genomic selection in plant breeding: knowledge and prospects. Adv Agron 2011;110:77-123.
59. Peleman JD, van der Voort JR. Breeding by design. Trends Plant Sci 2003;8(7):330-4.
60. Collard BCY, MacKill DJ. Marker-assisted selection: an approach for precision plant breeding in the twenty-first century. Phil Trans R Soc B 2008;363:557-72.
61. Morris GP, Ramu P, Deshpande SP, et al. Population genomic and genome-wide association studies of agroclimatic traits in Sorghum. PNAS 2013;110(2):453-58.
62. Thomson MJ. High-throughput SNP genotyping to accelerate crop improvement. Plant Breed Biotech 2014;2:195-212.
63. Bortesi L, Fischer R. The CRISPR/Cas9 system for plant genome editing and beyond. Biotechnol Adv 2015;33:41-52.
64. Wang Y, Cheng X, Shan Q, et al. Simultaneous editing of three homoeoalleles in hexaploid breadwheat confers heritable resistance to powdery mildew. Nat Biotechnol 2014;32:947-51.
65. Li T, Liu B, Spalding MH, et al. High-efficiency TALEN-based gene editing produces disease-resistant rice. Nat Biotechnol 2012;30:390-2.
66. Castaldini M, Turrini A, Sbrana C, et al. Impact of Bt corn on rhizospheric and soil eubacterial communities and on beneficial mycorrhizal symbiosis in experimental microcosms. Appl Environ Microbiol 2005;71(11):6719-29.
67. Turrini A, Sbrana C, Nuti MP. Development of a model system to assess the impact of genetically modified corn and aubergine plants on arbuscular mycorrhizal fungi. Plant Soil 2005;266:69-75.
68. Glandorf DCM, Bakker PAHM, van Loon LC. Influence of the production of antibacterial and antifungal proteins by transgenic plants on the saprophytic microflora. Acta Bot Neerl 1997;46:85-104.
69. Streitwolf-Engel R, van der Heijden MGA, Wiemken A, et al. The ecological significance of arbuscular mycorrhizal fungal effects on clonal reproduction in plants. Ecology 2001;82:2846-59.
70. Cheplick GP. Effects of endophytic fungi on the phenotypic plasticity of Lolium perenne (Poaceae). Am J Bot 1997;84:34-40.
71. Cheplick GP. Host genotype overrides fungal endophyte infection in influencing tiller and spike production of Lolium perenne (Poaceae) in a common garden experiment. Am J Bot 2008;95(9):1063-71.
72. Peiffer JA, Spor A, Koren O, et al. Diversity and heritability of the maize rhizosphere microbiome under field conditions. PNAS 2013;110(16):6548-53.
73. Pérez-de-Castro AM, Vilanova S, Cañizares J, et al. Application of genomic tools in plant breeding. Curr Genom 2012;13:179-95.
74. Tsaftaris AS, Polidoros AN, Kapazoglou A, et al. Epigenetics and plant breeding. Plant Breed Rev 2008;30:49-177.
75. Lynch M. Evolution of the mutation rate. Trends Genet 2010;26(8):345-52.
76. Rosenberg E, Zilber-Rosenberg I. Role of microorganisms in adaptation, development, and evolution of animals and plants: the hologenome concept. In: Rosenberg E, DeLong EF, Stackebrandt E, et al. (eds). The Prokaryotes -Prokaryotic Biology and Symbiotic Associations. Berlin Heidelberg: Springer-Verlag, 2013, 347-58.
77. Kiers ET, West SA, Denison RF. Mediating mutualisms: farm management practices and evolutionary changes in symbiont co-operation. J Appl Ecol 2002;39:745-54.
78. Kiers ET, Denison RF. Inclusive fitness in agriculture Inclusive fitness in agriculture. Philos Trans R Soc Lond B Biol Sci 2014;369(1642):20130367.
79. Sujay V, Gowda MVC, Pandey MK, et al. Quantitative trait locus analysis and construction of consensus genetic map for foliar disease resistance based on two recombinant inbred line populations in cultivated groundnut (Arachis hypogaea L.). Mol Breeding 2012;30(2):773-88.
80. Liao CY, Wu P, Hu B, et al. Effects of genetic background and environment on QTLs and epistasis for rice (Oryza sativa L.) panicle number. Theor Appl Genet 2001;103:104-11.
81. Acquaah G. Marker assisted selection. In: Acquaah G (ed). Principles of Plant Genetics and Breeding. Oxford, UK: John Wiley & Sons, 2012.
82. Capettini F, Rasmusson DC, Dill-Macky R, et al. Inheritance of resistance to Fusarium head blight in four populations of barley. Crop Sci 2003;43:1960-66.
83. Fountaina JC, Kheraa P, Yan L, et al. Resistance to Aspergillus flavus in maize and peanut: molecular biology, breeding, environmental stress, and future perspectives. Crop J 2015;3(3):229-37.
84. Lübberstedt T. Diagnostics in plant breeding. In: Lübberstedt T, Varshney R (eds). Diagnostics in Plant Breeding. Dordrecht, Netherlands: Springer, 2013, pp. 3-9. 9. Functional hologenomics in plant breeding | 295
85. Romagosa I, Fox P. Genotype × environment interaction and adaptation. In: Hayward MD, Bosemark NO, Romagosa I (eds). Plant Breeding: Principles and Prospects. London: Chapman and Hall, 1993, 373-90.
86. Becker HC, Leon J. Stability analysis in plant breeding. Plant Breeding 1988;101:1-23.
87. Soliman SSM, Trobacher CP, Tsao R. A fungal endophyte induces transcription of genes encoding a redundant fungicide pathway in its host plant. BMC Plant Biol 2013;13(1):93.
88. Ravi K, Vadez V, Isobe S, et al. Identification of several small main-effect QTLs and a large number of epistatic QTLs for drought tolerance related traits in groundnut (Arachis hypogaea L.). Theor Appl Genet 2011;122:1119-32.
89. Rehman AU, Malhotra RS, Bett K. et al. Mapping QTL associated with traits affecting grain yield in chickpea (Cicer arietinum L.) under terminal drought stress. Crop Sci 2011;51:450-63.
90. Varshney RK, Mohan SM, Gaur PM. Achievements and prospects of genomics-assisted breeding in three legume crops of the semi-arid tropics. Biotechnol Adv 2013; 31(8):1120-34.
91. Thudi M, Upadhyaya HD, Rathore A, et al. Genetic dissection of drought and heat tolerance in chickpea through genomewide and candidate gene-based association mapping approaches. PLoS ONE 2014;9(5):e96758.
92. Barbosa MAM, Lobato AKS, Yuen Tan DK, et al. Bradyrhizobium improves nitrogen assimilation, osmotic adjustment and growth in contrasting cowpea cultivars under drought. AJCS 2013;7(13):1983-89.
93. Lobato AKS, Silveira JAG, Costa RCL, et al. Tolerance to drought in leguminous plants mediated by Rhizobium and Bradyrhizobium. In: Akinci S (ed). Responses of Organisms to Water Stress. 2013. http://www.intechopen.com/books/responses-of-organisms-to-water-stress/tolerance-to-droughtin-leguminous-plants-mediated-by-rhizobium-and-bradyrhi zobium.
94. Sherameti I, Tripathi S, Varma A. The root-colonizing endophyte Pirifomospora indica confers drought tolerance in Arabidopsis by stimulating the expression of drought stressrelated genes in leaves. Mol Plant Microbe Interact 2008;21(6):799-807.
95. Kane KH. Effects of endophyte infection on drought stress tolerance of Lolium perenne accessions from the Mediterranean region. Environ Exp Bot 2011;71(3):337-44.
96. Nagabhyru P, Dinkins RD, Wood CL, et al. Tall fescue endophyte effects on tolerance to water-deficit stress. BMC Plant Biol 2013;13:127.
97. Hubbard M, Germida JJ, Vujanovic V. Fungal endophytes enhance wheat heat and drought tolerance in terms of grain yield and second-generation seed viability. J Appl Microbiol 2014;116(1):109-22.
98. Naveeda M, Mitter B, Reichenauer TG et al. Increased drought stress resilience of maize through endophytic colonization by Burkholderia phytofirmans PsJN and Enterobacter sp. FD17. Environ Exp Bot 2014;97:30-39.
99. Suman A, Shrivastava AK, Gaur A et al. Nitrogen use efficiency of sugarcane in relation to its BNF potential and population of endophytic diazotrophs at different N levels. Plant Growth Regul 2008;54(1):1-11.
100. Alberton O, Kuyper TW, Summerbell RC. Dark septate root endophytic fungi increase growth of Scots pine seedlings under elevated CO2 through enhanced nitrogen use efficiency. Plant Soil 2010;328:459-70.
101. Bakker PAHM, Ran LX, Pieterse CMJ, et al. Understanding the involvement of rhizobacteria-mediated induction of systemic resistance in biocontrol of plant diseases. Can J Plant Pathol 2003;25:5-9.
102. Bakker PAHM, Pieterse CMJ, Van Loon LC. Induced systemic resistance by fluorescent Pseudomonas spp. Phytopathology 2007;97:239-43
103. Bulgarelli D, Rott M, Schlaeppi K, et al. Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 2012;488:91-95.
104. Lundberg DS, Lebeis SL, Paredes SH, et al. Defining the core Arabidopsis thaliana root microbiome. Nature 2012;488:86-90.
105. Ofek M, Hadar Y, Minz D. Ecology of root colonizing Massilia (Oxalobacteraceae). PloS One 2012;7(7):e40117.
106. Vorholt JA. Microbial life in the phyllosphere. Nature Rev 2012;10:828-40.
107. Turnbaugh PJ, Ley RE, Hamady M, et al. The human microbiome project. Nature 2007;449:804-10.
108. Lundberg DS, Lebeis SL, Paredes SH, et al. Defining the core Arabidopsis thaliana root microbiome. Nature 2012;488:86-90.
109. Otani S, Mikaelyan A, Nobre T, et al. Identifying the core microbial community in the gut of fungus-growing termites. Mol Ecol 2014;23:4631-44.
110. Handelsman J. Metagenomics: application of genomics to uncultured microorganisms. Microbiol Mol Biol Rev 2004;68:669-85.
111. Krause A, Ramakumar A, Bartels D, et al. Complete genome of the mutualistic, N-2-fixing grass endophyte Azoarcus sp strain BH72. Nat Biotechnol 2006;24:1385-91.
112. Zuccaro A, Lahrmann U, Güldener U, et al. Endophytic life strategies decoded by genome and transcriptome analyses of the mutualistic root symbiont Piriformospora indica. PLoS Pathog 2011;7(10): e1002290.
113. Witzel K, Gwinn-Giglio M, Nadendla S, et al. Genome sequence of Enterobacter radicincitans DSM16656(T), a plant growth-promoting endophyte. J Bacteriol 2012;194(19):5469.
114. Kwak M-J, Song JY, Kim S-Y, et al. Complete genome sequence of the endophytic bacterium Burkholderia sp. strain KJ006. J Bacteriol 2012;194(16):4432-33.
115. Han JI, Choi HK, Lee SW, et al. Complete genome sequence of the metabolically versatile plant growth-promoting endophyte Variovorax paradoxus S110. J Bacteriol 2011;193(5):1183-90.
116. Mercado-Blanco J, Bakker PAHM. Interactions between plants and beneficial Pseudomonas spp.: exploiting bacterial traits for crop protection. Antonie Van Leeuwenhoek 2007; 92:367-89.
117. Hohnadel D, Meyer JM. Specificity of pyoverdine-mediated iron uptake among fluorescent Pseudomonas strains. J Bacteriol 1988;170(10):4865-73.
118. Fuchs R, Schäfer M, Geoffroy V, et al. Siderotyping-A powerful tool for the characterization of pyoverdines. Curr Top Med Chem 2011;1:31-35
119. Castillo UF, Strobel GA, Ford EJ, et al. Munumbicins, wide-spectrum antibiotics produced by Streptomyces NRRL 30562, endophytic on Kennedia nigriscans. Microbiol 2002;148(9):2675-85.
120. Sun H, He Y, Xiao Q, et al. Isolation, characterization, and antimicrobial activity of endophytic bacteria from Polygonum cuspidatum. Afr J Microbiol Res 2013;7(16):1496-504
121. Park J-K, Lee S-H, Han S. Marker-assisted selection of novel bacteria contributing to soil-borne plant disease suppression. In: de Bruijn FJ (ed). Molecular Microbial Ecology of the Rhizosphere, Vol. 2, 1st edn. New Jersey, USA: John Wiley & Sons Inc, 2013, 637-42.
122. McSpadden Gardener B, Weller D. Changes in populations of rhizosphere bacteria associated with take-all disease of wheat. Appl Environ Microbiol 2001;67:4414-25.
123. McSpadden Gardener B, Gutierrez L, Joshi R, et al. Distribution and biocontrol potential of phlD+ pseudomonads in corn and soybean fields. Phytopathology 2005;95:715-824
124. Tucci M, Ruocco M, De Masi L, et al. The beneficial effect of Trichoderma spp. on tomato is modulated by the plant genotype. Mol Plant Pathol 2011;12(4):341-54.
125. Ardanov P, Sessitsch A, Häggman H, et al. Methylobacterium-induced endophyte community changes correspond with protection of plants against pathogen attack. PLoS ONE 2012;7(10):e46802
126. Rengel Z, Marschner P. Nutrient availability and management in the rhizosphere: exploiting genotypic differences. New Phytol 2005;168:305-12.
127. Sidorova KK, Shumny VK, Vlasova YE, et al. Symbiogenetics and breeding of a macrosymbiont for increased nitrogen fixation capacity with special reference to the pea (Pisum sativum L.). Russ J Genet Appl Res 2011;1(1):73-87.
128. Wissuwa M, Mazzola M, Picard C. Novel approaches in plant breeding for rhizosphere-related traits. Plant Soil 2009;321:409-30
129. Kiers ET, Hutton MG, Denison RF. Human selection and the relaxation of legume defences against ineffective rhizobia. Proc Natl Acad Sci USA 2007;274:3119-26.
130. Kiers ET, Duhamel M, Beesetty Y, et al. Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 2011;333:880-2.
131. Herridge DF, Danso SKA. Enhancing crop legume NT fixation through selection and breeding. Plant Soil 1995;174:51-82.
132. Devine TE, Kuykendall LD. Host genetic control of symbiosis in soybean (Glycine max L.) Plant Soil 1996;186:173-87
133. Herridge DF, Turpin JE, Robertson MJ. Improving nitrogen fixation of crop legumes through breeding and agronomic management: analysis with simulation modelling. Aust J Exp Agric 2001;41:391-401.