Scholarly article on topic 'Scoping the potential uses of beneficial microorganisms for increasing productivity in cotton cropping systems'

Scoping the potential uses of beneficial microorganisms for increasing productivity in cotton cropping systems Academic research paper on "Biological sciences"

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Soil Biology and Biochemistry
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{Biofertilization / Biocontrol / Phytostimulation / PGP / Cotton}

Abstract of research paper on Biological sciences, author of scientific article — Lily Pereg, Mary McMillan

Abstract There is a growing body of evidence that demonstrates the potential of various microbes to enhance plant productivity and yield in cropping systems. Realizing the potential of beneficial microbes requires an understanding of the role of microbes in growth promotion, particularly in terms of fertilization and disease control, the underlying mechanisms and the challenges in application and commercialization of plant growth-promoting (PGP) microbes. This review focuses specifically on the use of PGP microbes in the cotton industry and summarizes the commercial bioinoculant products currently available for cotton; highlighting factors that must be considered for future development of PGP microbial products for the cotton industry. Given the paucity of information on beneficial microbes for cotton production systems in comparison to those for other cropping systems (e.g. legumes and grains), a snapshot of the current research is critical in light of the increased interest in cotton inoculants, mainly in developing countries such as India, and the overall increased interest in PGP applications as part of promoting sustainable agriculture.

Academic research paper on topic "Scoping the potential uses of beneficial microorganisms for increasing productivity in cotton cropping systems"

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Soil Biology & Biochemistry

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Scoping the potential uses of beneficial microorganisms for increasing productivity in cotton cropping systems

Lily Pereg*, Mary McMillan

School of Science and Technology, University of New England, Armidale, NSW 2351, Australia


Article history: Received 10 July 2014 Received in revised form 30 September 2014 Accepted 22 October 2014 Available online xxx







There is a growing body of evidence that demonstrates the potential of various microbes to enhance plant productivity and yield in cropping systems. Realizing the potential of beneficial microbes requires an understanding of the role of microbes in growth promotion, particularly in terms of fertilization and disease control, the underlying mechanisms and the challenges in application and commercialization of plant growth-promoting (PGP) microbes. This review focuses specifically on the use of PGP microbes in the cotton industry and summarizes the commercial bioinoculant products currently available for cotton; highlighting factors that must be considered for future development of PGP microbial products for the cotton industry. Given the paucity of information on beneficial microbes for cotton production systems in comparison to those for other cropping systems (e.g. legumes and grains), a snapshot of the current research is critical in light of the increased interest in cotton inoculants, mainly in developing countries such as India, and the overall increased interest in PGP applications as part of promoting sustainable agriculture.

© 2014 Published by Elsevier Ltd.

1. Introduction

Agricultural industries such as the cotton industry rely heavily on the use of chemical fertilizers, herbicides and pesticides. One of the aims of agricultural biotechnology is to develop microbial inoculants to enhance plant growth and suppress plant disease, with a key goal of reducing reliance on chemical fertilizers and pesticides (Adesemoye et al., 2009). Many factors need to be taken into consideration during the development of such inoculants commercially (Berg, 2009) including selection of appropriate plant growth-promoting (PGP) microbes based on target host plant, soil type, indigenous microbial communities, environmental conditions, inoculant density, suitability of carriers and compatibility with integrated crop management.

Plant growth and productivity is heavily influenced by the interactions between plant-roots and the surrounding soil, including the microbial populations within the soil. The plant rhizosphere harbours microorganisms that may have positive, negative or no visible effect on plant growth. Although most rhizospheric microbes appear to be benign, deleterious microorganisms include pathogens and microbes producing toxins that inhibit root growth or those that remove essential substances from the soil. By contrast

* Corresponding author. Tel.: +61 2 6773 2708; fax: +61 2 6773 3267. E-mail address: (L. Pereg). 0038-0717/© 2014 Published by Elsevier Ltd.

the main mechanisms for plant growth promotion include suppression of disease (biocontrol); enhancement of nutrient availability (biofertilization); and production of plant hormones (phytostimulation) (reviewed by Martinez-Viveros et al., 2010; Bhattacharyya and Jha, 2012). Studies of PGP microbes indicate that multifunctionality is a hallmark of the most beneficial (Vassilev et al., 2006; Avis et al., 2008).

The indigenous rhizospheric microbial population of agricultural soils is greatly influenced by agricultural practices (e.g. soil cultivation, season, stubble retention, burning etc.), crop plant species, cultivar and genotype, as well as soil type (Berg and Smalla, 2009; Reeve et al., 2010). Plant exudates may cause changes to soil characteristics such as pH and carbon availability, impacting the diversity and activity of microbial populations (Haichar et al., 2008). Bioaugmentation, the addition of microbes to agricultural soils, thus becomes a valuable influence on soil microbial processes.

In light of this, the question under consideration is the potential for successful application of biofertilization, biocontrol and phy-tostimulation in cotton production systems. This review summarizes the types of PGP microbes and the mechanisms by which they enhance plant growth, with particular attention to those tested on cotton, and discusses the factors essential to the practical application and commercialization of microbial inoculants for cotton. In addition, currently available commercial PGP and biocontrol products for cotton production systems are evaluated.

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2. Plant growth promotion in cotton: biocontrol, biofertilization and phytostimulation

2.1. Mechanisms of disease suppression

Globally, crop growth protection and health is continuously challenged by emerging, re-emerging and endemic plant pathogens (Miller et al., 2009). Chemical pesticide and fungicide use has led to environmental concerns and pathogen resistance, forcing constant development of new agents (Fernando et al., 2006). Rhi-zospheric microbes that suppress plant pathogens could be used as biocontrol agents, and may be considered as alternative to chemical pesticides. There are a number of mechanisms for plant pathogen suppression including direct inhibition of pathogen growth through production of antibiotics, toxins, hydrogen cyanide (HCN) and hydrolytic enzymes (chitinases, proteases, lipases) that degrade virulence factors or pathogen cell-wall components (reviewed in Whipps, 2001; Compant et al., 2005).

Antibiotics are a normal part of the self-protective arsenals of bacteria, such as Pseudomonas species (e.g. Pseudomonas fluorescens strains) (Haas and Defago, 2005) and Bacillus species (e.g. Bacillus subtilis) (Kim et al., 2003), as well as fungal species such as Tri-choderma, Gliocladium, Ampelomyces and Chaetomium (Kaewchai et al., 2009) and therefore these organisms have great potential for soil conditioning. Multifunctional organisms such as Tricho-derma harzianum Rifai 1295-22 appear to enhance plant growth by solubilising phosphate (P) and micronutrients required by plants, such as iron and manganese, and also suppresses plant pathogens (Altomare et al., 1999). HCN production suppresses microbial growth and may inhibit pathogens such as root-knot, bacterial canker and black rot in tomato and tobacco (Voisard et al., 1989; Siddiqui et al., 2006; Lanteigne et al., 2012). However HCN might be harmful to plants by inhibiting energy metabolism and reducing root growth (Siddiqui et al., 2006). Many different bacterial genera produce HCN, including Alcaligenes, Aeromonas, Bacillus, Rhizobium and Pseudomonas spp. (Ahmad et al., 2008).

Pathogen suppression can also occur competitively through indirect inhibition. Selected bacteria and fungi produce side-rophores as iron chelating agents especially during iron deficiency (Sharma and Johri, 2003), including Bradyrhizobium, Pseudomonas, Rhizobium, Streptomyces, Serratia, and Azospirillum (Martinez-Viveros et al., 2010). Their ability to deplete iron from their surroundings makes it unavailable to pathogenic fungi, creating a competitive advantage (O'Sullivan and O'Gara, 1992; Loper and Henkels, 1999). Inoculation with siderophore-producing bacteria grown under iron limiting conditions has a positive effect on plant growth (Carrillo-Castaneda et al., 2002); however the potential role for a combination of several PGP mechanisms and not siderophore production alone cannot be discounted.

Other mechanisms involved in disease suppression include activation of the plant's own defence system, known as induced systemic resistance (ISR). Volatile compounds released by PGP bacteria and fungi can trigger ISR, resulting in enhanced expression of defence-related genes in the host (Ryu et al., 2005; Hossain et al., 2007; Naznin et al., 2014).

2.2. Microbes that suppress disease in cotton

Cotton pathogens present a high economic burden to growers (Pereg, 2013). Seedling disease complexes are caused by several fungal and bacterial pathogens including Pythium ultimum, Rhizoctonia solani, Fusarium spp., Verticillium spp., Thielaviopsis basicola and Xanthomonas camprestris pv. malvacerum (Xcm). Management strategies to prevent disease include selection of suitable varieties and planting times, crop rotation with non-host

Table 1

Biocontrol agents identified to control common cotton pathogens.

Biocontrol agent

Pathogen/s controlled (geographic region)


Trichoderma virens Pythium ultimum (USA)

Rhizoctonia solani (USA) Fusarium oxysporum Verticillium dahliae Pseudomonas Pythium ultimum


Rhizoctonia solani verticillium dahlia

Xanthomonas camprestris (Xcm) (India) Pythium ultimum (USA) Rhizoctonia solani (USA) Rhizoctonia solani (Israel) Fusarium oxysporum Rhizoctonia solani (Argentina) Fusarium oxysporum Verticillium dahliae

Streptomyces lydicus Burkholderia cepacia Trichoderma harzianum Cladorrhium

foecundissimum Bacillus subtilis

Howell, 1982; Howell and Stipanovic, 1983; Howell, 2002 Howell et al., 2000 Zhang et al., 1996a Hanson, 2000

Howell and Stipanovic, 1980; Loper, 1988; Hagedorn and Nelson, 1990; Howie and Suslow, 1991; Loper, 1988 Howell and Stipanovic, 1979 Mansoori et al., 2013; Erdogan and Benlioglu, 2010 Habish, 1968; Mondel et al., 2000, 2001

Yuan and Crawford, 1995 Zakiet al., 1998 Elad et al., 1980 Sivan and Chet, 1986 Gasoni and Stegman de Gurfinkel, 2009 Zhang et al., 1996a Mansoori et al., 2013

species, optimised seed bed preparation and irrigation schedules, agrochemicals and improved farm-hygiene practices. Unfortunately, quite often fungicides are not effective against soil-borne pathogens and management strategies that control disease caused by one pathogen not only may not be effective in controlling others but might actually increase damage by other pathogens (Pereg, 2013). Disease-resistant cotton varieties with increased resistance to Fusarium and Verticillium spp. have been selected (Kappelman, 1980; Gore et al., 2009). While pathogen-specific resistance can be incredibly valuable, this is too restrictive in the face of the number of cotton pathogens, and commercial transgenic varieties with resistance to multiple soil-borne diseases are currently unavailable. Despite attempts to develop such resistant variants, cotton seedling disease remains an ongoing issue for producers. Consequently the studies that have identified PGP microbes with potential as biocontrol agents against common cotton pathogens (see Table 1) provide an important alternative.

A number of organisms can cause damping-off in cotton, resulting in substantial losses to growers. P. ultimum soil infestation is one such organism, but research has demonstrated that several rhizospheric microbes have an antagonistic effect against P. ultimum infection in cotton, such as Entobacter cloacae and Erwinia herbicola (Nelson, 1988). The fungus Trichoderma (Gliocladium) virens improves the survival of cotton seedlings, possibly due to the production of the antibiotic compound gliovirin (Howell, 1982; Howell and Stipanovic, 1983). Several Trichoderma spp. control the disease by competing for metabolites released from the germinating seeds (Howell, 2002). P. fluorescens increases seedling survival and cotton stand in P. ultimum infested soil, possibly through antibiosis and antagonistic siderophore production (Howell and Stipanovic, 1980; Loper, 1988; Hagedorn and Nelson, 1990; Howie and Suslow, 1991). Streptomyces lydicus can destroy germinating oospores and damage the cell walls of fungal hyphae, making it a potential biocontrol agent against Pythium seed and root rot in cotton and other crops (Yuan and Crawford, 1995).

Similarly R. solani also plays a critical role in the pronounced losses due to cotton damping-off. Seed treatment with a P. fluorescens strain from the rhizosphere of cotton seedlings, or pyrrolnitrin, an antibiotic produced by P. fluorescens, greatly increased seedling survival in R. solani infested soils. Pyrrolnitrin

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1 also inhibits growth of other pathogenic fungi including T. basicola rhizosphere (Richardson et al., 2009). Microorganisms play an 66

2 and Verticillium dahliae (Howell and Stipanovic, 1979). In field trials, important role in the soil phosphorus cycle and, thus, in mediating 67

3 a soil drench of Burkholderia cepacia improved plant stand in phosphorus availability to plants, enhancing the capacity of plants 68

4 R. solani infested soils, possibly due to the production of growth- to acquire phosphorus from the soil by directly solubilising and 69

5 inhibiting antifungal compounds (Zaki et al., 1998). Trichoderma mineralising inorganic phosphorus or by facilitating the mobility of 70

6 spp. including T. harzianum and Trichoderma virens have been organic phosphorus through microbial turnover and/or increasing 71

7 identified as biocontrol agents against R. solani (Elad et al., 1980). the root system (Richardson and Simpson, 2011). Myriad soil mi- 72

8 Interestingly, T. virens controls R. solani through induction of the crobes that solubilise inorganic phosphorus have been isolated, 73

9 plant's defence response, whereas its control of another pathogen, including bacteria such as Actinomycetes, Pseudomonas, Rhizobium 74

10 P. ultimum, is through antibiotic production (Howell et al., 2000). and Bacillus spp. (Richardson et al., 2009; Richardson and Simpson, 75

11 The endophytic fungus Cladorrhinum foecundissimum colonises 2011; Bhattacharyya and Jha, 2012). In addition, some fungal 76

12 cotton seedling roots and reduces disease incidence amongst plants members of the Penicillium genus excrete organic acids that facili- 77

13 transplanted into R. solani infested soils (Gasoni and Stegman de tate the conversion of immobilised soil phosphorus into soluble 78

14 Gurfinkel, 2009). forms available to plants (Wakelin et al., 2004). 79

15 Numerous Fusarium spp. have been found to be associated with The rate of root growth and the plasticity of root architecture 80

16 cotton seedling roots, however only some species are pathogenic, along with the development of the rhizosphere, through either root 81

17 causing Fusarium wilt (Zhang et al., 1996b). T. harzianum controls growth or extension of root hair, are clearly important for effective 82

18 Fusarium wilt in both naturally and artificially Fusarium oxysporum exploration of soil and interception of nutrients. Root hair can 83

19 infested soils and persists in the soil through consecutive plantings, constitute up to 70% of root volume and may absorb up to 80% of 84

20 reducing disease incidence at each planting (Sivan and Chet, 1986). phosphorus in non-mycorrhizal plants (Fohse et al., 1991). Mycor- 85

21 Growth chamber and greenhouse experiments have demonstrated rhizal fungi colonise the root cortex and extend externally, con- 86

22 that both T. virens and B. subtilis reduce seedling colonisation and necting the roots with surrounding soil and increasing efficiency of 87

23 supress the incidence and severity of wilt (Zhang et al., 1996a). phosphorus acquisition by mycorrhizal plants (Barea et al., 2008). 88

24 Cotton-associated bacteria including Aureobacterium sapardae, Ba- Mycorrhizal symbiosis may potentiate plant growth through 89

25 cillus pumilus, Pseudomonas putida and Burkholderia solanacearum enhancement of plant establishment, protection against stress, 90

26 also reduce disease severity in F. oxysporum infected cotton (Chen improved soil structure and increased nutrient uptake, particularly 91

27 et al., 1995). phosphorus and essential micronutrients, such as Zn, Cu (and also 92

28 Although the pathogenic fungus Verticillium dahlia causes Ver- other nutrients such as Mg, Ca and K, depending on soil pH) (Clark 93

29 ticillium wilt, one of the most important cotton diseases, and Zeto, 2000; Richardson et al., 2009). 94

30 P. fluorescens and Bacillus spp. strains reduce its incidence when 95

31 applied to cotton seeds before planting in V. dahlia inoculated soil 2.4. Microbial fertilization in cotton production 96

32 (Mansoori et al., 2013). Further, treatment with Pseudomonas spp., 97

33 T. virens or Enterobacter sp. HA02 decrease wilt incidence and Over the past decade the number of field and laboratory 98

34 improve cotton growth parameters (Hanson, 2000; Erdogan and studies on PGP microbial inoculants for cotton has grown 99

35 Benlioglu, 2010; Li et al., 2012). Similarly, mycorrhizal fungi of (Table 2), with several studies focusing on co-inoculation with 100

36 Glomus spp. including G. etunicatum can diminish the symptoms of multiple organisms. Various N-fixing, P-solubilising and indole-3- 101

37 Verticillium cotton wilt under controlled conditions (Kobra et al., acetic acid (IAA)-producing bacteria from Azotobacter, Azospirillum, 102

38 2009). Acetobacter and Pseudomonas genera have been used as inoculants 103

39 Xcm, a cause of bacterial cotton blight, is also suppressed by P.under irrigation. Multiple strains increased boll number and 104

40 fluorescens (Habish, 1968), potentially through production of weight, and could promote this increased yield under reduced 105

41 growth-inhibiting antimicrobial compounds (Mondel et al., 2000, levels of chemical fertilization (Narula et al., 2005). Gomathy et al. 106

42 2001). (2008) found that using a mix of Azospirillum, Methylobacterium 107

43 and P-solubilising Bacillus spp. in combination with NPK fertil- 108

44 2.3. Mechanisms of biofertilization ization significantly increased cotton growth and yield in field 109

45 trials under drip irrigation. Co-inoculation of fields with Azospir- 110

46 Biofertilizers are microorganisms that enhance nutrient avail- illum sp., P-solubilising bacteria and methylotrops significantly 111

47 ability to plants, contributing to plant nutrition either by facilitating enhances root and shoot growth, fibre yield, and, to some extent, 112

48 nutrient uptake or by increasing primary nutrient availability in the fibre quality when used in combination with fertilizers (Dhale 113

49 rhizosphere. They might also be used to increase crop yield when et al., 2010, 2011), as well as increased yield under reduced 114

50 applied complementary to, or as replacement for, chemical levels of chemical fertilizers (Nalayini et al., 2010). Similarly, 115

51 fertilizers. treatment of cottonseeds with a mixture of Pseudomonas aerugi- 116

52 Nitrogen (N) is an essential plant nutrient that is often limited in nosa Z5 and Bacillus fusiformis S10 isolated from cotton in Pakistan 117

53 agricultural soils due to high losses by emission or leaching. N improved yield of cotton under reduced fertilizer conditions 118

54 fixation can be carried out by non-symbiotic bacteria such as Azo- (Yasmin et al., 2013). 119

55 spirillum, Burkholderia, Gluconacetobacter and Pseudomonas species Several biofertilizers have been tested individually. The strain 120

56 (Dobbelaere et al., 2003), and may be used in biofertilization of and the type of formulation of P. fluorescens was shown to impact 121

57 non-leguminous crops such as rice (Mirza et al., 2006; the ability of the bacterium to promote plant growth. Strain Q18 122

58 Muthukumarasamy et al., 2007), sugarcane (Suman et al., 2005, was more effective than strain CKK-3, and utilising bentonite as a 123

59 2008), wheat (Egamberdiyeva and Hoflich, 2002) and maize mineral carrier promoted greater seedling height and root length 124

60 (Estrada et al., 2005). The Azotobacter strain Azo-8 was also found than talc or organic carriers such as peat and rice bran (Ardakani 125

61 to be effective as bio-inoculant for wheat grown under dryland et al., 2010). In addition, the potassium-mobilizing bacterium Ba- 126

62 conditions in combination with urea and manure (Singh et al., cillus edaphicus enhanced the root and shoot growth of seedlings in 127

63 2013). pot trials of cotton grown in potassium-deficient soil and increased 128

64 Although soils generally contain substantial total phosphorus, the N and P concentration in plants through root proliferation 129

65 available phosphorus is often quickly depleted from the (Sheng, 2005). 130

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Table 2

PGP microbial inoculants beneficial to cotton in field and laboratory trials conducted over the last decade.

Microbial inoculant

Experimental system



Azotobacter, Azospirillum, Acetobacter and

Pseudomonas spp. Coinoculation of Azospirillum, Methylobacterium,

P-solubilising Bacillus spp. Coinoculation of Azospirillum, methylotrops, P-solubilising bacteria

Coinoculation of Azospirillum, methylotrops,

P-solubilising bacteria Pseudomonas aeruginosa Z5 + Bacillus fusiformis S10

Pseudomonas fluorescens

Bacillus edaphicus Raoultella planticola

Azotobacter chroomcoccum + mycorrhizal fungi

Irrigated field cotton

Field inoculation under drip irrigation

Applied on top of seeds, cotton fields under irrigation

Field trials in winter irrigated cotton

Applied as seed coating and tested in field trials

Greenhouse trials using different formulations for application Greenhouse pot trials Pot trials, saline soils

Seed treatment, field trials

Increased boll number and weight; reduced chemical fertilization Increased growth and yield when combined with chemical fertilizer Enhanced root and shoot growth, fibre yield and quality when combined with chemical fertilizer Increased cotton yield with reduced application of chemical fertilizer Improved growth and yield with reduced application of chemical fertilizer

Promoted plant growth, type of formulation important Increased root and shoot growth Enhanced seed germination, increased plant height and weight Improvement in plant height, boll number and boll weight. Synergistic effect of coinoculation

Narula et al., 200S Gomathy et al., 2008 Dhale et al., 2010, 2011

Nalayini et al., 2010 Yasmin et al., 2013

Ardakani et al., 2010

Sheng, 200S Wu et al., 2012

Paul et al., 2011

2.5. Mechanisms of phytostimulation

One of the most important mechanisms of plant growth promotion is the production of plant hormones, or phytostimulation, by some rhizospheric microorganisms. PGP microbes enhance plant growth by producing growth hormones, such as auxins, gibberellins and cytokinins in the proximity of the roots, or by controlling the levels of ethylene produced by plants. The size and depth of root systems influence the capacity of plants to efficiently capture nutrients from soil and vice versa: root growth and morphology may change in response to nutrient availability (Wijesinghe et al., 2001). Having both shallow and deep roots allows the plant to reach both mineralized nitrogen available in topsoils, for example, as well as leached nitrogen in the depth (Gastal and Lemaire, 2002; Ho et al., 2005). Consequently, using phytostimulation for enhancing plant root development could play a significant role in improving nutrient uptake, especially if applied in combination with biofertilization.

1AA, the main plant auxin, stimulates root growth and shapes architecture (e.g., lateral root initiation, root vascular tissue development, root hair positioning) (Aloni et al., 2006). Many different rhizobacteria, including pathogenic, beneficial, associative and free living, are able to produce 1AA (Tsavkelova et al., 2006). Examples include Azospirillum, Aeromonas, Azotobacter, Bacillus, Burkholderia, Enterobacter, Pseudomonas and Rhizobium (Spaepen et al., 2006; Martinez-Viveros et al., 2010). Cytokinins stimulate plant cell division and control root development by inhibiting primary root elongation and lateral root formation and promoting root hair formation (Werner et al., 2003; Riefler et al., 2006). They are produced by some PGP rhizobacteria, such as Arthrobacter, Azospir-illum, Pseudomonas and Paenibacilus species, but their involvement in plant growth promotion is not well understood (Richardson et al., 2009). Similarly, gibberellins promote the development of stem tissue, root elongation and lateral root extension (Barlow et al., 1991; Yaxley et al., 2001), and are produced by species of PGP rhizobacteria, such as Azospirillum, Azotobacter, Bacillus, Her-baspirillum, Gluconobacterand Rhizobium (MacMillan, 2002; Bottini et al., 2004).

Ethylene is an important plant hormone essential for plant growth and development, although it may have different effects on plant growth depending on its concentrations in plant roots (Pierik et al., 2006). Ethylene is required for the induction of systemic resistance during interaction with associative microbes, and higher

concentrations are involved in plant defence in response to pathogen infection (Broekaert et al., 2006). Certain PGP bacteria, such as Azospirillum brasilense, can produce small amounts of ethylene, which may promote root hair development (Ribaudo et al., 2006). Ethylene is produced in plants from the substrate 1-aminocyclopropane-l-carboxylate (ACC), which is released by plants into the rhizosphere in times of stress, and reabsorbed by the roots to be converted to ethylene. However, ethylene accumulation in the roots causes reduced root growth, exacerbating plant stress (Babalola, 2010). Rhizospheric PGP fungi and bacteria (e.g. P. putida) that can degrade ACC reduce the adsorption of ethylene by the roots and allow the plant to re-establish a healthy root and cope with environmental stress (Glick, 2005). Plant growth promotion by ACC degrading microbes seems to be particularly important under stress such as cold, drought, saline soils or flooded soils contaminated by heavy metals (Grichko and Glick, 2001; Mayak et al., 2004). Microbes able to degrade ACC include Achromo-bacter, Azospirillum, Bacillus, Enterobacter, Pseudomonas and Rhizobium strains (Martinez-Viveros et al., 2010).

2.6. Phytostimulation in cotton

Table 2 also summarises recent field and laboratory studies on phytostimulation for cotton, conducted in the last decade. Many inoculants (see section 2.4), such as Azospirillum and Pseudomonas spp. have multiple beneficial traits. Differentiating between plant growth promotion due to phytostimulation versus biofertilization can be accomplished by examining whether mutant strains deficient in plant hormone production are still able to promote plant growth. For example, Azospirillum brasilense mutants with reduced levels of 1AA production are affected in their ability to promote wheat growth (Dobbelaere et al., 1999; Spaepen et al., 2008). 1AA and ACC deaminase production by the rhizobacterium Raoultella planticola as well as enhanced uptake of N, P and other nutrients are the mechanisms suggested for the increased germination rate, height and weight in cotton seedlings observed under salinity stress (Wu et al., 2012). The 1AA producing bacterium Azotobacter chroomcoccum, particularly when co-inoculated with arbuscular mycorrhizal fungi, improved seed germination, seedling development, plant height, boll number and boll weight when applied as a seed treatment (Paul et al., 2011).

Soil aggregation is also important for allowing root penetration and soil aeration, as well as infiltration and retention of water,

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1 leading to improved plant growth (Miller and Jastrow, 2000). Ex- R. solani, especially when combined with chemical fungicides (Zaki 66

2 amples of microbes that could contribute to the formation of soil et al., 1998). 67

3 aggregates in cotton growing soils are arbuscular mycorrhiza It is recognized that evaluation and ranking of P-solubilising and 68

4 (Rillig, 2004) and exopolysaccharide-producing bacteria such as N-fixing microbes under laboratory conditions do not necessarily 69

5 Azospirillum, which can attach to soil particles depending on soil correspond to the efficiency of the PGP microbe for enhancing P or 70

6 type and overall conditions (Bashan, 1999). N uptake under field conditions (Martinez-Viveros et al., 2010). The 71

7 production of plant growth hormones that improve root surface 72

8 3. Considerations for use and commercialisation of PGP area may improve the ability of the plant to absorb these and other 73

9 microbes for cotton production nutrients from the rhizosphere (Khalid et al., 2004); therefore, it 74

10 would be beneficial to utilise those biofertilizers that can undertake 75

11 Although many microbes have been demonstrated to stimulate dual actions - solubilise/mineralise P and/or fix N as well as 76

12 plant growth and yield in the laboratory, the results have been stimulate roots growth or mycorrhizal formation that enhance the 77

13 poorly repeatable in field trials (Bhattacharjee et al., 2008; adsorption of these nutrients from the rhizosphere (Vassilev et al., 78

14 Martinez-Viveros et al., 2010), creating a barrier to commerciali- 2006). Alternatively, the use of compatible inoculant mixes could 79

15 zation and widespread use (Richardson et al., 2009). Further serve the same purpose. There is evidence from trials in cotton that 80

16 progress in this area depends on a clear understanding of the fac- co-inoculation with multiple PGP microbes can increase plant yield 81

17 tors that influence the efficacy of microbial inoculants in the field, compared to single inoculums (Paul et al., 2011; Yasmin et al., 2013). 82

18 including plant species, soil type, local microbial communities, In addition, the use of multiple biocontrol agents can overcome 83

19 environmental conditions, inoculant carrier and other manage- some of the variability observed in field trials and broaden the 84

20 ment practices such as fertilization, cultivation, irrigation and pest environmental conditions under which a biocontrol agent can be 85

21 control. Together, plant species and soil type shape microbial used (Guetsky et al., 2001). Given the aforementioned cotton 86

22 communities in the rhizosphere (Garbeva et al., 2004; Berg and growth conditions, it would be beneficial to utilize PGP microbes 87

23 Smalla, 2009), and this must be taken into consideration when that have been implicated in stress protection, perhaps in 88

24 introducing microbial inoculants. Plant root exudates affect the conjunction with other biological agents. Studies have already 89

25 surrounding soil, and can impact the ability of different microbial identified microbes that improve cotton growth and yield under 90

26 species to colonise and thrive in the rhizosphere (Rovira, 1969). Soil conditions of potassium-limitation (Sheng, 2005) and saline stress 91

27 type and farm management practices also have a great influence on (Wu et al., 2012), and further research into these microbes and their 92

28 rhizospheric microbe populations (Reeve et al., 2010), with nutrient possible inclusion in a bio-inoculant seems warranted. 93

29 availability such as N and P, different pH, moisture content varying Microbial inoculants have numerous advantages when 94

30 widely across soil types, with divergent capacities to support compared with chemical fertilizers, fungicides and pesticides: 95

31 colonisation and growth of microbes. Indeed, Neumann et al. (2011) through careful selection of suitable microbes there is a reduced 96

32 demonstrated that soil factors had a much greater influence on the risk of environmental damage and potentially human health; they 97

33 growth of alfalfa than inoculation with PGP microbes. The are safer to apply; their activity is more targeted; they are effec- 98

34 composition of indigenous microbial communities within soils will tive in small quantities; they are able to multiply given appro- 99

35 also impact the ability of introduced microbes to effectively colo- priate conditions (where their population size is controlled by the 100

36 nise the rhizosphere in sufficient numbers to effect plant growth plant and indigenous microbes) and may survive to the next 101

37 (van Veen et al., 1997). Competition with the resident flora could season; they decompose faster and more effectively; and they can 102

38 rapidly deplete the population of introduced microbes, and may be used on their own or in combination with conventional pest 103

39 account in part for the inconsistencies observed between green- management (Berg, 2009). When used together with chemical 104

40 house studies and field trials (Martinez-Viveros et al., 2010). fertilisers, it would be necessary to define the most effective ratio 105

41 The majority of cotton production takes place in arid or semi- between inoculum size and the concentration of fertilisers. 106

42 arid soils, which poses additional challenges for the design and Management strategies combining pesticides or herbicides 107

43 use of bio-inoculants (Bashan, 1998). Low rainfall and high tem- application and bio-inoculants must test for resistance of the bio- 108

44 peratures characterize arid or semi-arid regions and soils in these inoculant to the agrochemicals and for optimal methods of co- 109

45 regions are often nutrient poor, are prone to salinity and often application. 110

46 contain high amounts of insoluble P, with only approximately 2-4% In addition to the ecological considerations outlined above, 111

47 available for plants (Richardson et al., 2009). These factors must be there are also economic and manufacturing factors that need to 112

48 taken into consideration when selecting bio-inoculants, especially be taken into account with regards to the commercialization of 113

49 for dryland cotton, as introduced microbes must have the ability to microbial inoculants. The mass production of microbes can be 114

50 colonise and promote plant growth under these environmental technically challenging and expensive; products need to be 115

51 conditions. Delivery methods and the nature of the carrier also formulated to have long shelf life (transport and storage), which 116

52 need to be optimized to assure rapid colonization of target plants, may be problematic in particular with gram-negative bacteria 117

53 as the harsh conditions in these regions can quickly diminish the that do not form spores. Further, registration procedure can be 118

54 population of introduced microbes (Bashan, 1998), with techno- expensive and time consuming, and application must be both 119

55 logical advances targeting efficient delivery of bio-inoculants in simple and compatible with agronomic practices and equipment 120

56 crop production systems (Carr et al., 2014). (Berg, 2009; Kaewchai et al., 2009; Figueiredo et al., 2010). A 121

57 Indigenous strains of rhizobacteria, isolated from the intended study into the adoption of biological inputs in cotton production 122

58 plant and better adapted to the local environment, may have more in India showed that some of the factors influencing the usage of 123

59 competitive power and be more effective as bio-inoculants (Khalid bio-inoculants included concerns about timely availability and 124

60 et al., 2004). The importance of increasing the fitness of the reduced shelf life of bio-inoculants, and cumbersome application 125

61 biocontrol agent in the field was highlighted in field tests in Ari- methods (Sundaravardarajan et al., 2006). The success of the 126

62 zona, where the effectiveness of Burkholderia cepacia, locally iso- biocontrol agent Kodiak® in cotton production may be largely 127

63 lated from cotton fields was compared with that of several attributed to its integration with standard chemical fungicides, 128

64 commercial products, including Kodiak® and Deny®. The local allowing for ease of application and long-term activity (Brannen 129

65 strain showed the most effective control of damping-off caused by and Kenney, 1997). 130

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3.1. Commercial PGP and biocontrol products for use in cotton production

The increased research focus on PGP microbes has led to the commercialization of a number of products for use in the agricultural industry. This section examines the commercial products marketed for use on cotton specifically or on all agricultural soils/ crops including cotton.

In 1992, B. subtilis GB03 was registered as a commercial biocontrol product for cotton pathogens in the USA, named Kodiak® (Gustafson Inc. USA). The development of the biocontrol agent used in Kodiak® originated in Australia (1970s to late 1980s) with B. subtilis (isolate A-13), which was well documented as a biocontrol and growth promoting agent in wheat and peanut, leading to the cotton-adapted strain GB03 used in Kodiak® (Brannen and Kenney, 1997). Kodiak® works as a biocontrol against Rhizoctonia and Fusarium spp. Mahaffee and Backman (1993) found that cotton seed-factors, including surface pH, cultivar, and presence of fungicide coating, influenced the colonization of cotton and its rhizo-sphere by this biocontrol agent; thus, such factors have to be considered when developing an inoculant product for cotton.

Current products in the USA include Ascend™ PA, a biofertilizer containing the mycorrhizal fungi Glomus intraradicies, and the information provided suggests that it increases growth in cotton by 300% (BioScientific, Inc., Arizona, USA, PIX PLUS® combines Bacillus cereus with mepiquat chloride, and is marketed to increase boll number and size, increasing yield by up to 82lb/acre on average (Arysta LifeScience, USA, Deny® (Stine Microbial Products, USA) and Intercept® (Soil Technologies Corp., USA) are two biocontrol products marketed for use on cotton and a variety of other crops, which contain Burkholderia cepacia, and are used for the control of Rhizoctonia, Pythium and Fusarium spp.. SoilGard® (Certis Inc., USA) is marketed for the control of Pythium, Rhizoctonia and Fusarium spp., through the active agent Trichoderma virens. Contans® WG (Prophyta Biologischer Pflanzenschutz GmbH, Germany) is a Coniothyrium minitans-containing biocontrol agent active against Sclerotinia sclerotiorum and S. minor in all susceptible crop species including cotton. Afla-Guard® (Syn-genta Crop Protection Inc., USA) contains Aspergillus flavus NRRL 21882, which acts to control aflatoxin-producing fungal pathogens in a wide range of crop species including cotton.

In Australia current products include BioAg Soil and Seed® (BioAg, AU, for improvement of soil fertility, promotion of rapid seed germination and early root development. This formulation can be applied via irrigation or used as a seed inoculant. Table 3 summarises currently available commercial bio-inoculants for use in cotton production systems.

In addition to commercial products currently in use there are also a number of other microorganisms registered with the U.S. Environmental Protection Agency as biopesticides (http://iaspub. The Arizona Cotton Research and Protection Council (USA) has registered A. flavus AF36 as a biopesticide to control the growth of aflatoxin-producing A. flavus on cotton.

4. Summary and conclusions

Plant growth promotion is a complex phenomenon rarely attributable to a single mechanism as most PGP microbes influence plant growth through multiple mechanisms, and in some cases their PGP effect may only occur through interactions with other microbes. Any microbial agent added to the rhizosphere has to interact not only with the plant but also with any other organism sharing the same ecological niche. To be successful the inoculant has to maintain a critical population mass in the soil and have the right conditions to exert its beneficial activity.

Despite the challenges, a growing variety of microorganisms with properties that can be exploited in plant growth promotion are being discovered and tested under field conditions, with the number of successful cases increasing. The direct benefits of such research are both financial, from reductions in the use of chemical fertilizers and pesticides, and productive through improved crop yield, while indirect benefits include reduced toxin accumulation in agricultural soils and reduced environmental pollution with agricultural runoff. Success is often associated with a combination of inoculants possessing complementary beneficial traits, e.g. bio-fertilizers that increase nutrient availability in the proximity of the roots together with a mycorrhizal fungus that enhances the root system and assists the plant to absorb the nutrients. It is not surprising that often indigenous microbes prove the most effective; such microbes suit the environmental conditions in the cropping system for which they are intended. Nevertheless, indigenous microbes would still have to out-compete other microbes for resources and, in the case of biocontrol agent, suppress pathogens.

The Australian cotton industry is one industry that could greatly benefit from research into isolation of crop-specific beneficial microbes. In general, it can be said that similar groups of beneficial microbes seem to be involved in promoting the growth of different plants, with examples including bacteria from the Bacillus, Azo-spirillum, Pseudomonas groups and mycorrhizal fungi. Nevertheless, there is sufficient evidence to suggest that particular microbial species, or even strains, benefit specific plants under defined conditions; thus there is a need to carry out region specific research to produce inoculants specific to the crop, agronomic practices, soil type and other environmental conditions.

In addition to isolating microbial agents for augmentation, further research should be directed into cropping practices that enhance both existing and introduced beneficial microbes, such as controlling the amount of chemical inputs, as over-application of chemicals may suppress the activity of beneficials and increase the

Table 3

Commercial biocontrol and biofertilizer products currently marketed for use in cotton production.

Commercial product PGP microbe Use Company

Kodiak Bacillus subtillus GB03 Control of Fusarium and Rhizoctonia spp. Gustafson Inc, USA

Ascend/BuRIZE Glomus intraradicies Increases cotton growth Bioscientific Inc., USA

PIX PLUS Bacillus cereus Increase boll number and size Arysta LifeScience, USA

Deny Burkholderia cepacia Control of Rhizoctonia, Fusarium and Pythium spp. Stine Microbial Products, USA

Intercept Burkholderia cepacia Control of Rhizoctonia, Fusarium and Pythium spp. Soil Technologies Corp., USA

SoilGard Trichoderma virens Control of Rhizoctonia, Fusarium and Pythium spp. Certis Inc., USA

Contans WG Coniothyrium minitans Control of Sclerotinia spp. Prophyta Biologischer Pflanzenschutz

GmbH, Germany

Afla-Guard Aspergillus flavus NRRL 21882 Control of aflatoxin-producing fungi Syngenta Crop Protection Inc, USA

BioAg Soil and Seed Unspecified Improve soil fertility and promote rapid seed BioAg, Australia

germination and early root development

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activity of detrimental microorganisms. Consequently there is great scope for collaborations to develop technology to screen for and identify microbes with beneficial traits; assess the benefit to the plant; test strains for commercialization; design the best formulations for inoculant delivery; detect and assess the performance of inoculants in the soil; analyze soil microbial communities and the effects of the soil inoculation on soil health; and study the general effects of cropping practices on specific microbial communities.

Molecular techniques, such as proteomics and transcriptomics, add a new dimension to the understanding of the overall responses of plants and pathogens during disease cycles (Nittler et al., 2005; Coumans et al., 2009, 2010, 20И). Such information can be useful in the development of disease control measures, including biocontrol. Genome analysis can indicate the presence of virulence genes and transcriptome analysis can determine the expression of such genes, allowing for the screening of virulence suppressive factors. In searching for new PGP traits, it is possible to screen the genomic library of certain beneficial microbial species, e.g. P. fluorescens, for sequences that may be involved in plant growth promotion (Berg, 2009).

Soil microbial diversity analysis (e.g. DNA-microarrays and pyrosequencing) under different crop management strategies can supply information about the presence of pathogens and/or PGP microbes in the rhizosphere, while methods such as qRT-PCR and RNA sequencing can supply information on the active growth of different microbes, and whether specific functional genes are being expressed. Such modern techniques can be used in promoting crop production practices that enhance PGP activity in the soil, reducing nutrient removal (e.g. denitrification) and suppressing pathogen virulence. Natural disease suppressive soils, where disease suppression is due to biological factors, can give clues as to the structure of microbial communities associated with disease suppression. Such soils have also a good potential to be a source of biocontrol agents.

While microbial communities and their functions can be studied using molecular techniques, culturing techniques need to be employed in the isolation of PGP microbes. Such methods vary and are dependent on the mechanism sought after and the biology of the microorganism. The development of biocontrol agents requires vigorous screening. There is no defined screening for biocontrol agent as it depends on the crop, the affected part of the plant, the target pathogen, and the cropping system. Observation of zones of pathogen growth inhibition led to the identification of many useful bacterial biocontrol agents, although this method does not identify biocontrol agents with other modes of action such as induced systemic resistance or competition (McSpadden et al., 2002). As previously mentioned, indigenous and suppressive soils could be good sources of PGP microbes; however, current techniques for initial screening of pathogen suppressive microbes are very labor intensive and new, more direct ways of isolating beneficial microbes from soils are required.

Pathogen suppressive parasites may be isolated from buried propagules of the pathogen retrieved from the soil. Microbes controlling pathogen populations by competition may be those that are fast colonizers of sterilized soil and can exclude growth of other organisms as well as looking for microbes that colonize the same niches as the pathogen.

In conclusion, the search for new biocontrol microbes is ongoing and gaining importance, as issues of pathogenic resistance grow in the face of increased need for crops commensurate with a growing world population. It is recognized that continued production of new biocontrol agents will be required to diversify the potential applications of biocontrol and in order to replace commonly used biocontrol products in case resistance develops. Consequently there is a pressing need for cross-disciplinary collaborations and a

better and more comprehensive understanding of soil— plant—microbe interaction.


This review is one of the outcomes of a project funded by the Q1 Australian Cotton Research and Development Corporation.


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