Chapter 3

Benefits of Breeding Crops for YieldResponse to Soil Organisms

Alison E. Bennett, Timothy J. Daniell, and Philip J. WhiteThe James Hutton Institute, UK

3.1 INTRODUCTION

The Agrarian Revolution is considered to have begunapproximately 10,000 years ago and is associated withthe transition of human communities from hunting andgathering to settlement and agriculture (Fig. 3.1). Over themillennia since then, the domestication of wild species, theselective breeding of high yielding genotypes, and numer-ous technological advances have enabled the productionof edible crops to increase and thus support the nutritionalrequirements of a global population of over 7 billion peo-ple (FAO, 2012). In the recent past, during the periodknown as the Green Revolution (1950–present), crop pro-duction increased dramatically (Fig. 3.1; FAO, 2012). Thiswas founded mainly on the development of semi-dwarfcereal crops and crops resistant to pests and pathogens,whose yields are maintained through the application ofagrochemicals to control weeds, pests, and diseases, min-eral fertilizers, and irrigation (Evans, 1997; Godfray et al.,2010; Fageria et al., 2011; White et al., 2012). In recentdecades, the consumption of natural resources to deliverfertilizers, agrochemicals, and clean water to agriculture,and to build and maintain the infrastructures required forcrop production has accelerated (Fig. 3.1; FAO, 2012).This has incurred increasing economic and environmen-tal costs (Nellemann et al., 2009; Rockstrom et al., 2009;Vitousek et al., 2009; White and Brown, 2010; Dawsonand Hilton, 2011; White et al., 2012). It is now evidentthat if agriculture is to support the human populations pre-dicted for the next decades through the millennia ahead,more sustainable strategies for crop production must bedeveloped (Graham et al., 2007; White and Brown, 2010).

Molecular Microbial Ecology of the Rhizosphere, Volume 1, First Edition. Edited by Frans J. de Bruijn. 2013 John Wiley & Sons, Inc. Published 2013 by John Wiley & Sons, Inc.

It is hoped that the beneficial relationships between cropplants and their symbionts, and their combined influenceon the biology, chemistry, and physics of the rhizosphereand soil can be exploited for this sustainable intensifi-cation of crop production (Graham et al., 2007; Fageriaet al., 2011) to create a new revolution in crop production,which is referred to as the Evergreen Revolution (Fig. 3.1).

Plants, agricultural and otherwise, associate with awide variety of soil organisms. These associations areoften ignored because they are not easily visible, yet soilorganisms can influence the phytoavailability and uptakeof water and essential mineral elements by plants, whichin turn can influence plant growth and crop yield (Morganet al., 2005). Modern agricultural practices have, for themost part, eliminated the dependence on soil organisms byproviding plant nutrients, pathogen defense, and herbivoredefense with inputs of mineral fertilizers and agrochemi-cals. However, as peak oil and peak phosphorus begin tolimit the availability of inorganic fertilizers and syntheticagrochemicals (Raven, 2008; Cordell et al., 2009; Dawsonand Hilton, 2011), agriculture will need to employ moresustainable means of crop production.

The future sustainability of agricultural productionwill depend more upon utilizing positive associationswith soil organisms while avoiding negative associations.For example, a wide variety of different soil organismscan increase the phytoavailability of essential mineralnutrients. Mutualists such as mycorrhizal fungi andrhizobia can acquire essential mineral elements that oftenrestrict crop production, such as phosphorus (P) andnitrogen (N), and deliver them directly to their host plants,whereas free-living organisms such as those involved in

17

18 Chapter 3 Benefits of Breeding Crops for Yield Response to Soil Organisms

Mycorrbizal response

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(b) Figure 3.1 (a) Schematic representations of globalhuman population (black line), global cerealproduction (red line), global consumption ofN-fertilizers (green line), P-fertilizers (blue line), andagrochemicals (purple line) during the AgrarianRevolution and the Green Revolution (1950–2010)and their projections for the future based onbusiness-as-usual (dotted lines) or the adoption ofmore sustainable practices (Evergreen Revolution;dashed line). (b) Schematic representations of“boom-and-bust” cycles in crop losses to pathogens(purple line), response of crop yield to AM-fungi(blue line), and biological nitrogen fixation inagriculture (green line).

nitrogen or phosphorus cycling influence the phytoavail-ability of nutrients in the rhizosphere and, thereby, havethe potential to increase crop yields. However, plantinteractions with soil organisms are not always beneficial.For example, nitrogen- and phosphorus-cycling organ-isms can reduce the phytoavailability of these elementsand encourage their losses from agricultural systems.Additionally, pathogens, parasites, and root herbivorescan reduce plant biomass directly and impact crop yieldnegatively. The interactions between plants and soilbiota can be influenced dramatically by managementpractices. For example, high levels of plant availablenutrients reduce the colonization of crops by mycorrhizalfungi and rhizobia, which can have unpredictable conse-quences for soil biota, soil chemistry, and soil physicalproperties.

Plants can associate with soil organisms with bothpositive and negative effects and it is the net effect ofthese associations that will ultimately determine cropyield. To date, it has remained impossible to dissectthe complex interactions among soil communities thatresult in variations in crop yields. However, a commonmethod to assess the magnitude of these interactions isto determine the response of the system to perturbation.The term “response” was first coined to describe theinfluence of arbuscular mycorrhizal (AM) fungi on plantgrowth among multiple plant species (Plenchette et al.,1983; Hetrick et al., 1990). However, this variable hasbeen expanded to describe the influence of a wide variety

of soil organisms, either individually or collectively,on plant growth and crop yields (e.g., Vandegehuchteet al., 2010; Bennett et al., 2011). There are severaldifferent metrics for response (Righetti et al., 2007), butall measure the variation between growth in the presenceor absence of a test organism.

In this chapter we focus on the response of plantsto three commonly studied groups of soil organisms(pathogens, AM fungi, and rhizobia) that have thepotential to exert strong influences on crop production.We describe the interactions between these organisms andcrop plants, and their potential influence on crop yields.We also examine how breeding might have influenced theresponses of crop plants to these organisms to provideinsight to the potential of using these organisms toimprove crop production with reduced agricultural inputs.

The first group of soil organisms we consider issoil pathogens. These attack crop species and result inreduced crop yields. Extensive efforts have been made tobreed crops for resistance to soil pathogens. When resis-tant genotypes are not available, soil pathogens can becontrolled by agronomic practices such as the applicationof agrochemicals (fungicides, pesticides, insecticides),soil ameliorants to modify soil pH, fertilizers to maintainplant vigor, or irrigation, as in the case of common scabof potatoes.

The second group of soil organisms we consider isAM fungi, which can supply essential mineral elements

3.2 Has Breeding Reduced The Yield Response of Crops to pathogens? 19

with restricted phytoavailability, such as P and micronu-trients, to the host plant in exchange for carbon (Morganet al., 2005; Smith and Read, 2008; see Chapter 43). As aresult, AM fungi could play a big role in the P nutrition ofplants, and in P cycling within agricultural fields, therebycontributing to sustainable crop P nutrition. In addition,AM fungi have been shown to improve plant water uptake(Smith and Read, 2008), reduce the impact of pathogens(Borowicz, 2001; Pozo and Azcon-Aguilar, 2007), andalter plant secondary chemistry (Gange and West, 1994;Bennett et al., 2009). Despite the many potential benefitsof AM fungi, the actual outcome of an association witha host plant depends greatly on specific interactions withdifferent AM fungal species and the phytoavailability ofphosphorus (Smith and Read, 2008).

The third group of soil organisms we consider arenitrogen fixing bacteria (such as rhizobia, bradyrhizobia,and azorhizobia), which are commonly utilized to supple-ment N-fertilizer additions in agriculture (Fageria et al.,2011; White et al., 2012; see Section 6). These bacte-ria inhabit nodules that form in the roots or the stemsof legume species, and fix atmospheric nitrogen for theirplant hosts. The N fixed by rhizobia can increase N supplynot only to the host legume but also to the intercroppedplants and to the subsequent crops in rotations. The utiliza-tion of nitrogen-fixing bacteria should reduce the require-ment for N-fertilizers in agriculture, although there willstill be an absolute requirement for chemical inputs tomaintain sufficient crop production for the world’s humanpopulation, if it follows current trajectories (Graham et al.,2007; Erisman et al., 2008; Dawson and Hilton, 2011;Fig. 3.1). Today, it is estimated that biological nitrogen-fixation inputs 50–70 Tg N annual to agricultural systems(Herridge et al., 2008), which compares to approximately100 Tg N per year produced through the Haber–Boschprocess and applied as inorganic N-fertilizer (Fig. 3.1;Gruber and Galloway, 2008).

3.2 HAS BREEDING REDUCEDTHE YIELD RESPONSE OF CROPSTO PATHOGENS?

Potential losses due to pathogens have been estimatedto be about 9–21% of global crop production (Oerke,2006), but global losses due to specific root pathogenshave rarely been estimated. Pathogens have the greatesteffect in monoculture systems when adaptation to over-come resistance in a common crop genotype can havecatastrophic effects, as illustrated by the Great Irish PotatoFamine (Lucas, 1998).

Before monocultures of a single crop genotypebecame popular it is assumed that instances of catas-trophic losses in crop productivity resulting from the

overabundance of a particular pathogen were rarer, lessintense, and likely driven by local dynamics (Fig. 3.1).The severity and frequency of individual outbreaks ofdisease, root and otherwise, likely increased due tothe introduction of monocultures, resulting in regular“boom-and-bust” yield cycles linked to breeding cycles.In these cycles, breeders discover genetic resistance toa pathogen (or pathogen strain), introduce a resistantgenotype leading to increased crop productivity, then apathogen capable of overcoming crop resistance evolves,which results in renewed crop losses. For example, theGreat Irish Potato Famine of the 1850s led to a widesearch for genotypes and species of potato resistant toPhytophthora infestans, the cause of the famine (Lucas,1998). Researchers eventually developed resistant geno-types by creating hybrids between the common potato,Solanum tuberosum, and wild relatives such as Solanumdemissum and Solanum berthaultii (Lucas, 1998). Theinitial resistant varieties were grown widely until theirresistance was overcome by another strain of P. infestansleading to renewed crop losses. The cycle of selectionfor genotypes of cultivated potato with resistance to P.infestans and the subsequent evolution of P. infestans toovercome crop resistance continues today.

During the Green Revolution, farmers began com-bining the cultivation of crop genotypes with resistanceto pathogens with an increased use of agrochemicalsto reduce losses from pests and diseases (Fig. 3.1).Today, root pathogens are still controlled through thistwo-pronged approach: application of fungicides andbreeding for resistance. Modern breeding for resistanceto root pathogens takes a more active role than merelyselection and mating of resistant and susceptible geno-types. Molecular tools have grown in use, and the use ofirradiation, cell culture, and direct genetic manipulationhave all been used to breed crop genotypes resistantto root pathogens (Niks et al., 2011). In addition, croppathologists have taken prescient strategies to breedingfor resistance. Instead of breeding for resistance to asingle threat, they now try to anticipate threats to producecrop genotypes with resistance to multiple pathogens orstrains of pathogens that will exhibit resilience in theface of multiple threats (Niks et al., 2011). Thus, croppathologists are trying to breed for a reduction in thefrequency and amplitude of cycles of crop losses frompathogens, and are becoming increasingly successfulwhen these efforts are combined with applications ofeffective agrochemicals. Nevertheless, this is a relentlesstask and if applications of agrochemicals become limitedin the future, crop pathologists will have a greater chal-lenge to breed crops for stability of yields in monocultureagriculture. If they continue to be successful, we canexpect current levels of pathogen control to be main-tained; but if their breeding efforts cannot compensate

20 Chapter 3 Benefits of Breeding Crops for Yield Response to Soil Organisms

for the likely reduction in agrochemical inputs, we mightexpect to see more frequent and catastrophic crop losses(Fig. 3.1).

3.3 HAS BREEDING REDUCEDTHE YIELD RESPONSE OF CROPSTO AM FUNGI?

3.3.1 Genetic Variation inResponse to AM Fungi amongCrop SpeciesUnlike the situation for pathogens, there has not been anydirected breeding effort to influence interactions betweenplants and AM fungi. As a result, there is very little his-torical literature investigating changes in the response ofcrop plants to AM fungi. Indeed, the study of AM fungihas a relatively short history of about 100 years (Smithand Read, 2008), which is significantly shorter than thelength of time the pathogens have been observed and stud-ied (centuries). However, it seems likely that breedingefforts, particularly modern breeding efforts, have selectedfor crop plants with a reduced response to AM fungi—atrait that may pose problems in the future if the availabilityof P fertilizers becomes limiting.

In order for breeding to select for a reduced responseto AM fungi, there must be genetic variation within cropspecies for this trait. To our knowledge, response to AMfungi has not been tested directly in the founder popula-tions of any crop species. However, variation in responseto AM fungi has been demonstrated among genotypesof cultivated crops and in natural populations of speciesin a number of different ways. For example, variationin response to AM fungi has been reported among nearisogenic lines derived from four Trifolium repens parents(Eason et al., 2001) and among genotypes of severalMedicago spp. (Monzon and Azcon, 1996). Variation inresponse to AM fungi has also been found between intro-duced and native genotypes of Hypericum perforatum(Seifert et al., 2009), suggesting that selective pressurescan act on introduced species in their new range to altertheir response to AM fungi. Similarly, the invasive grassHolcus lanatus was shown to have a smaller response toAM fungi despite a higher level of AM fungal coloniza-tion than the native plant Erigeron glaucus in a Californiancoastal prairie (Bennett et al., 2011). Studies of H. lanatusin its native European habitat revealed a different patternin which H. lanatus responds positively to AM fungi andits soil community (Bischoff et al., 2006; Macel et al.,2007). This supports the hypothesis that introduced plantspecies can experience selective pressures that reduce theirresponse to AM fungi. Finally, it has been demonstratedin six Plantago lanceolata genotypes that variation in

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Figure 3.2 The relative growth of six Plantago lanceolatagenotypes with three fungal inocula (Glomus white, Acaulosporatrappei , and Scutellospora calospora).

response to a single AM fungal species is correlated withresponse to any other AM fungal species regardless of thetotal benefit provided by the AM fungal–plant combina-tion (Fig. 3.2). There was variation in the response of P.lanceolata genotypes to different fungal species, but plantgenotypes that attained the highest biomass with one fun-gal species also attained the highest biomass with everyother species. This result suggests that plant responseto one community of AM fungi is correlated with plantresponse to any other AM fungal community. While allthese studies were conducted in greenhouse settings, anal-ogous results have been obtained under field conditions(Pringle and Bever, 2008). We therefore conclude that (i)variation in natural plant populations for responsivenessto AM fungi exists, (ii) selection on responsiveness toAM fungi can occur, and (iii) selection in host plantsin response to one AM fungal community will likelyinfluence response to other AM fungal communities.

Although the founder populations of crop plantshave, to our knowledge, never been tested for theirresponse to AM fungi, we can base predictions aboutthe propensity for variation in response to AM fungiin particular crop species on phylogenetic comparisons(Fig. 3.3). Wilson and Hartnett (1998) examined 99plant species from a prairie habitat and observed greatvariation in their response to AM fungi. These plantspecies and their response to AM fungi can be placedon a phylogenetic tree along with the 21 most importantcrop species (Fig. 3.3). From this analysis, the responseto AM fungi of particular plant species can be predicted.For example, it can be observed that grasses from the

3.3 Has Breeding Reduced The Yield Response of Crops to am Fungi? 21

Figure 3.3 Phylogenetic distribution of mycorrhizal responsiveness (%) among the angiosperm families surveyed by Wilson and Hartnett(1998). Values are means of data for the number of species (n) surveyed in each plant family, with the exception of values for the Poaceae,which are means of data for the number of species (n) surveyed in each tribe. The phylogenetic position of the 21 most important crops basedon world production figures for 2010 (FAO, 2012) are also indicated. The phylogenetic tree is based on that of The Angiosperm PhylogenyGroup III (2009).

subfamily Pooidae (tribes Aveneae, Bromeae, Poeae, andTriticae) tend to have a low response to AM fungi. Thisobservation is consistent with many independent studies.Nevertheless, even in species from these clades, geneticvariation in response to AM fungi has been reported.For example, variation in response to AM fungi hasbeen shown repeatedly among wheat genotypes (Junand Allen, 1991; Hetrick et al., 1992, 1993, 1996; Yaoet al., 2001a, 2001b), although older wheat cultivarshave been shown to have a greater response to AM fungithan recent cultivars (Kapulnik and Kushnir, 1991; Zhuet al., 2001). Variation among genotypes in response toAM fungi has also been demonstrated in barley (Zhuet al., 2003) and pearl millet (Krishna et al., 1985).To add further weight to assertion that responsivenessto AM fungi is a genetic trait and can be selectedupon, wheat genes responding to colonization by AMfungi have been identified on chromosomes 5 and 7

in the B and D genomic backgrounds (Hetrick et al.,1995).

In contrast to the grasses discussed earlier, grassesfrom the Chloridoideae subfamily (tribes Cynodonteae,Eragrostideae, and Zoysieae) and the Panicoideae sub-family (tribes Andropogonodae and Paniceae) tend torespond strongly to AM fungi (Fig. 3.3). This has beenconfirmed in several studies of maize genotypes (Khalilet al., 1994; Al Karaki and Al Raddad, 1997; Kaeppleret al., 2000; Karasawa et al., 2001; Singh et al., 2002;Shah et al., 2006; dos Reis et al., 2008). In addition,significant variation in root colonization by AM fungihas been demonstrated among 100 maize genotypes, withvariation being greatest among land races and hybrids(An et al., 2010). These observations suggest that thereis inherent genetic variation across the breeding historyof maize for association with, and potential response to,AM fungi. Variation in response to AM fungi among

22 Chapter 3 Benefits of Breeding Crops for Yield Response to Soil Organisms

genotypes has also been demonstrated in sorghum,a member of the Andropogonodae (Mehraban et al.,2009). This research supports the notion that there isgenetic variation in response to AM fungi among cerealcultivars derived from founder Poaceae populations thatcan be selected upon to improve yield response to AMfungi.

The majority of research on the responses of cropspecies to AM fungi has been conducted on cereal crops.However, there is also much research documentingvariation in the response to AM fungi among genotypesof other major plant families and crop species. Forexample, within the Fabaceae there is a great rangeof response to AM fungi. This family contains speciesthat respond strongly to AM fungi as well as thenon-responding species (Wilson and Hartnett, 1998),resulting in a predicted medium level of response for thefamily as a whole (Fig. 3.3). Variation in response to AMfungi among genotypes of several crop species in theFabaceae has been documented. These species includechickpea (Cicer arietinum; El Ghandour et al., 1996;Konde and Deshmukh, 1996), lentil (Lens culinaris;Krishnareddy and Ahlawat, 1996), groundnut/peanut(Arachis hypogaea; Daft, 1991; Ibrahim et al., 1995), andsoybean (Glycine max; Khalil et al., 1994).

Although there are few agricultural species in theAsteraceae, and none in the list of 21 most importantcrops (FAO, 2012), this family contains many horticulturalspecies. From the data of Wilson and Hartnett (1998), thisfamily is predicted to have a medium level of responseto AM fungi (Fig. 3.3). Studies of a horticultural species,marigold (Tagetes spp.), have supported the prediction ofresponsiveness to AM fungi and also demonstrated varia-tion among genotypes (Linderman and Davis, 2004).

Although the study by Wilson and Hartnett (1998)investigated the AM responsiveness in a great number ofdifferent families and phylogenetic groupings, it did notinclude all of the phylogenetic groupings we might con-sider important for agriculture (Fig. 3.3). For example, nospecies from the Solanaceae were contained in the survey.However, there have been several studies on the responseto AM fungi of crop species of the Solanaceae thathave shown variation among genotypes including studieson tomato (Solanum lycopersicum; Bryla and Koide,1998, Al Karaki et al., 2001), Solanum aethiopicum (acrop grown in Africa) (Diop et al., 2003), and pepper(Capsicum annuum; Sensoy et al., 2007). The Rutaceaegenotypes from several citrus species have shownvariation in their response to AM fungi (Graham et al.,1997).

Unfortunately, not all plant families were well rep-resented in the study of Wilson and Hartnett (1998). Forexample, only one member of the Rosaceae was testedand it was reported to respond negatively to AM fungi.

However, strawberry, also a member of the Rosaceae, gen-erally responds strongly to AM fungi, but also varies inthe magnitude of its response (Vestberg, 1992). For severalof the less commonly cultivated plant species, it is diffi-cult to make predictions about their responsiveness to AMfungi. However, genotypes of sesame (Sesamum indicum;Sulochana et al., 1989), acerola (Malpighia emarginata;Costa et al., 2001), mulberry (Morus spp.; Venkatara-mana et al., 2007), grapevine (Vitis vinifera; Lindermanand Davis, 2001), and papaya (Carica papaya; Trindadeet al., 2001) all vary in their response to AM fungi. Thus,we can conclude that (i) variation in response to AMfungi is a widespread trait likely to occur in all cultivatedcrop species, (ii) the potential magnitude of responsive-ness of a particular species can be predicted by knowledgeof the responsiveness of wild or cultivated relatives, and(iii) variation in response to AM fungi is a genetic traitthat can be selected upon.

3.3.2 Breeding for Response to AMFungi in Crop SpeciesResponse to AM fungi is not a trait for which breedershave intentionally selected when developing new varieties.Instead, any selection on response to AM fungi by cropspecies has been unintentional and due to undirected selec-tion pressures. Researchers studying AM fungi generallyagree on three undirected selection pressures in the breed-ing process that disturb the AM fungal–plant mutualism,and could result in selection for reduced response to AMfungi: soil disturbance, high nutrient availability (particu-larly of phosphorus), and monoculture.

The AM fungal hyphal network in soil acquiresnutrients for host plants, transfers carbon between hosts(Smith and Read, 2008), and is a form of fitness for manyAM fungal species that preferentially colonize hosts fromhyphae as opposed to spores (Smith and Read, 2008).However, physical disturbance of the soil, such as occursduring tilling, breaks up this hyphal network limiting theability of AM fungi to gather nutrients for host plantsand transfer carbon between hosts, and, in some species,eliminates their ability to colonize new host plants. Asa result, plants grown in tilled soils are less likely toencounter AM fungi than plants grown in undisturbedenvironments, and lack of AM fungal associations, inparticular with a diversity of AM fungi, might limit plantgrowth and crop yields.

When the phytoavailability of mineral nutrients, espe-cially P, is high, AM fungi still colonize host plant roots,but no longer provide a benefit. Instead, they become acarbon drain on their host and are considered to be par-asitic (Smith and Read, 2008). Thus, in well-fertilizedagricultural systems, plant genotypes that can limit theirassociation with AM fungi are likely to perform best. High

3.4 Has Breeding Reduced The Yield Response of Crops to Rhizobia? 23

soil fertility can also affect AM fungal community struc-ture by selecting for types that might not provide a positivebenefit when mineral nutrients are in short supply.

Finally, AM fungal diversity and plant diversity aremaintained in nature by plant–soil negative feedback pro-cesses, which lead to temporal variation in the abundanceof AM fungal and plant species (Bever et al., 2001).As a result, multiple plant species are needed to main-tain multiple AM fungal species in the system and viceversa. However, in monocultures there are no multipleplant species, and evidence from invasive species thatform monocultures has demonstrated that, as a force ontheir own, monocultures reduce AM fungal abundance anddiversity (Vogelsang and Bever, 2009). Thus, plants grownin monoculture are likely to encounter mainly AM fungalspecies, which can tolerate monocultures and not necessar-ily the diversity of AM fungal species required to supporthigh crop yields.

In general, soil disturbance, fertilization, and mono-cultures appear to have reduced AM fungal diversityin intensive agricultural systems (Daniell et al., 2001)although organic systems often exhibit a higher diversityof AM fungi (Oehl et al., 2004). As the majority ofcrop species are bred and tested in dense monoculturesin disturbed soils that are fertilized, elite genotypes arebeing selected in an environment where they neither neednor are likely to encounter a diversity of beneficial AMfungi. Thus, it would not be surprising if crop genotypeswith reduced responses to, or associations with, AMfungi have been selected during the breeding process. Ifthis were true, one might expect to see a greater responseto AM fungi in land races and older crop genotypesthan in more recent genotypes. Consistent with thishypothesis, comparisons of modern and older maizecultivars have demonstrated that the greatest variation inroot colonization by AM fungi occurs among land racesand hybrids (An et al., 2010) and older cultivars of wheathave been shown to have a greater response to AM fungithan modern cultivars (Kapulnik and Kushnir, 1991; Zhuet al., 2001). Thus, recent breeding efforts appear to havereduced the response of cereals to AM fungi, a trend thatmight have to be reversed if we are to achieve sustainablecrop production in the future. However, in contrast tothese conclusions, a recent meta-analysis, focused onwhether crop breeding had selected for reduced responseto AM fungi, concluded that the response of crop plantsto AM fungi had not been influenced by crop breeding(Lehmann et al., 2012). However, this meta-analysisdid not incorporate phylogenetic effects. As we havealready discussed, phylogenetic effects have a stronginfluence on plant response to AM fungi (Fig. 3.3).Lehmann et al. (2012) lumped all grasses together as lowresponders despite having both low and high respondinggrass species in their data set. Ignoring phylogenetic

effects is likely to have compromised the conclusionsof the meta-analysis, especially if different groups arerepresented in a nonuniform pattern, as admitted byLehmann et al. (2012). As a result, more meta-analysesand examinations across the angiosperm phylogeny andthe breeding history of crop plants for responses toAM fungi are required to describe the variation in plantresponse to AM fungi adequately.

3.4 HAS BREEDING REDUCED THEYIELD RESPONSE OF CROPS TORHIZOBIA?

To our knowledge, variation in the response of founderpopulations of legume crops to rhizobial colonizationhas not been estimated. However, variation in responseto rhizobia (Yates et al., 2011) has been demonstratedin natural populations of legume species (e.g., Elliottet al., 2009) and there have been many studies describingvariation in response to rhizobia among cultivars andgenotypes of particular legume species (e.g., Chaverraand Graham, 1992; Abi-Ghanem et al., 2011; Biabaniet al., 2011; Paula Rodino et al., 2011). These studieshave identified various characteristics that are correlatedwith increased nitrogen fixation. For example, in commonbean (Phaseolus vulgaris) variation in nitrogen fixationhas been associated with early nodulation, for which thereis considerable genetic variation (Chaverra and Graham,1992), and with the size of root nodules (Paula Rodinoet al., 2011), and in peas and lentils increased nitrogenfixation is correlated with nodule number (Abi-Ghanemet al., 2011). Differences in such Characteristics can leadto considerable variation in nitrogen-fixing capabilityamong cultivars of legume crops.

There have been fewer comparisons of the response torhizobia of wild and bred genotypes of particular legumespecies. As a result, although there are suggestions ofreduced rhizobial association, and reduced nitrogen fixa-tion, among cultivated legumes, for example, in chickpea(Biabani et al., 2011), further evidence needs to be col-lected. It appears that many of the same selective pressuresinfluencing crop response to AM fungi, such as increasedsoil disturbance, high phytoavailability of nutrients andmonoculture, are likely to act as selection pressures in thelegume–rhizobia system. As rhizobia can live freely inthe soil without a host, the effects of tillage are likely tobe less severe for the legume–rhizobia association thanfor the AM fungal–plant association. However, soil dis-turbance, particularly burying of rhizobial cells deeper inthe soil during tillage, likely reduces encounters betweenhost plants and bacterial partners, thereby reducing theperiod of symbiotic nitrogen fixation in an annual crop.

24 Chapter 3 Benefits of Breeding Crops for Yield Response to Soil Organisms

Intensive agriculture with high N-fertilizer inputsreduces the dependence of legumes on biologicalnitrogen fixation. In addition, studies have shown thatgreater N phytoavailability reduces the efficacy of thelegume–rhizobia symbiosis by reducing overall nodula-tion as well as the level of nitrogen fixation per nodule(e.g., Hungria et al., 2006). When N-fertilizer inputsare high, genotypes with reduced rhizobial associationsare likely to have higher yields because they receivesufficient N and do not deliver C to rhizobia. Thus,selecting for increased yield in agricultural systems withhigh N-fertilizer inputs would inadvertently select forreduced rhizobial associations.

The response of rhizobia to monocultures isunknown, but it is known that multiple genotypes ofrhizobia can associate with a specific host plant. Cropspecies grown repeatedly in monoculture tend to havea greater specificity for particular rhizobial strains thannonagricultural species growing in more diverse plantcommunities (Provorov and Tikhonovich, 2003; Mutchand Young, 2004). This suggests that legume genotypesbred for improved yields when grown in monocultureare less able to support a diverse community of rhizo-bia, which might influence the efficacy of subsequentsymbiotic nitrogen fixation in arable fields.

Very clearly breeding and cultivation of legumesin systems with high N-fertilizer inputs has influencedlegume–rhizobia associations. Selection has acted ontraits associated with biological nitrogen fixation, such asearly nodulation (Chaverra and Graham, 1992), nodulenumber (Abi-Ghanem et al., 2011), and nodule biomass(Paula Rodino et al., 2011), but genetic variation in thesecharacteristics still persists. Breeding has resulted inlegume genotypes with a higher specificity for rhizobialsymbionts, which are then less able to associate withthe wider population of rhizobial strains found in nature(Provorov and Tikhonovich, 2003; Mutch and Young,2004). Thus, it is not surprising that researchers havebeen calling for breeding programs to focus on biologicalnitrogen fixation in legumes (Ranalli and Cubero, 1997;Herridge et al., 2008; Biabani et al., 2011), and identify-ing breeding strategies for increasing biological nitrogenfixation in agriculture (Barron et al., 1999).

Given the large genetic variation in response torhizobia within many legume species, the questionarises: Can breeding strategies be developed to increasebiological nitrogen fixation under field conditions and,thereby, reduce our dependence on the Haber–Boschprocess and synthetic N-fertilizers? The answer to thisquestion is unequivocally: Yes. This approach has beenled by Latin American countries, particularly Brazil andAustralia, who have created legume-breeding programsthat target increasing nitrogen fixation in legumes directly(Nicolas et al., 2002; Alves et al., 2003; Hungria et al.,

2005; Unkovich et al., 2008) and also investigate themanagement of external factors, such as the appropriateuse of rhizobial species for each soil type, to maximizethe benefit of biological nitrogen fixation to crop pro-duction (Hungria and Vargas, 2000). These breedingprograms have been quite successful, and have reducedthe need for N-fertilizer additions. As a result, breedingfor increased nitrogen fixation in leguminous species,with its application in both intercropping and rotations,appears to be a viable and sustainable strategy forreducing our dependence on synthetic N-fertilizers.

3.5 CONCLUSION

This chapter has described how breeding has influencedcrop responses to pathogens, AM fungi, and rhizobia.It has been observed that conventional breeding effortsappear to have selected for reduced responses to all threegroups of soil organisms, whether intentionally or uninten-tionally. Most people would agree that reduced responsesto pathogens provide a benefit, whereas reduced responsesto AM fungi and rhizobia, although having little effectunder current practices in intensive agriculture involvingtillage, fertilizer additions, and monoculture, might restrictfuture crop production should the availability of mineralfertilizers become limiting, or policy and environmentalpressures, such as the need for increased carbon storagein soils, alter tillage practices.

In the future, it is likely that sustainable mineral nutri-tion of crops will require beneficial relationships with soilorganisms such as AM fungi and rhizobia, and this willultimately influence breeding strategies. The major chal-lenge for breeders will be to reduce the detrimental effectsof pathogens while increasing associations with beneficialorganisms such as AM fungi and rhizobia. Superficially,this process seems simple enough. Breeders might developgenotypes resistant to pathogens with relatively high lev-els of association with AM fungi and rhizobia. However,AM fungi and rhizobia both trigger and then shut downthe salicylic acid pathway, which is a key determinant oftheir host plant’s response to pathogen infection. Theseeffects on the salicylic acid pathway could have variousconsequences. For example, genotypes bred for a reducedresponse to pathogens might also have reduced associa-tions with AM fungi and rhizobia (Toth et al., 1990) orcolonization by AM fungi and rhizobia might prime plantsfor faster responses to pathogens. Although we know ofno direct test of the first effect, there is evidence that bothAM fungi and rhizobia prime plant responses to pathogens(Pozo and Azcon-Aguilar, 2007; Zamioudis and Pieterse,2012), which can lead to reductions in pathogen infectionin hosts of both mutualists (Borowicz, 2001; Zamioudisand Pieterse, 2012). However, we do not know whether

References 25

changes in pathogen resistance influence associations withAM fungi or rhizobia or whether there is an interactionbetween pathogen resistance and the priming effects pro-duced by AM fungi and rhizobia.

If it is possible to breed for reduced responses topathogens together with increased response to AM fungiand rhizobia, then it might be possible to maintain, oreven increase, crop production in a future with reducedfertilizer and agrochemical inputs (Fig. 3.1). However,breeding efforts will need to begin soon. Restrictions onmany agrochemicals are already in place in the EU andelsewhere, peak phosphorus is expected to occur about2030, and the availability of fossil fuels to provide theenergy required for the Haber–Bosch process and thesynthesis of agrochemicals is likely to peak shortly after-ward (Raven, 2008). As a result, the general availabilityof fertilizers and agrochemicals is likely to decrease inthe immediate future, and breeding programs will need torespond equally quickly to identify crop genotypes thatyield well in a new agricultural environment.

ACKNOWLEDGMENTS

This work was supported by the Rural and EnvironmentScience and Analytical Services Division (RESAS)of the Scottish Government through Workpackage 3.3(2011–2016). We thank James D. Bever for assistance inthe development of Figure 3.2 and Euan James for hiscomments on the manuscript.

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