Plant basal resistance - Universiteit Utrecht

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Chapter 4 patterns, we considered the possibility that DIMBOA act as a chemo-attractant for P.putida. This hypothesis was confirmed by our subsequent chemotaxis assays, which demonstrated positive taxis of P. putida KT2440 towards DIMBOA (Figure 4). P. putida KT2440 is tolerant of DIMBOA in comparison to other soil bacteria (Figure 2A). We subsequently found that P. putida KT2440 accelerates decomposition of DIMBOA and its direct break-down product MBOA (Figure 2B), indicating BX catabolism (Kumar et al., 1993). Such a mode of tolerance is supported by our transcriptome analysis, which revealed seven DIMBOA-inducible genes that can be associated with degradation of N-heteroaromatic compounds (Table I). These genes include nuoCD (PP4121) and nuoG (PP4124), which encode subunits of NADH dehydrogenase I, PP4690 encoding a Rieske 2Fe-2S family subunit of soluble dioxygenases, PP0256 encoding a molybdopterin oxidoreductase, PP4661 encoding a putative oxidoreductase, and the α/β hydrolase-fold superfamily genes PP4540 and PP4551, members of which catalyse 1H-3-hydroxy-4-oxoquinoline degradation by P. putida 33/1 (Fischer et al., 1999). We conclude that this mechanism of BX tolerance provides P. putida KT2440 with a competitive advantage over other micro-organisms in exploiting the maize rhizosphere. Our soil-based colonisation essays revealed that P. putida cells colonise maize roots of DIMBOA-producing lines in greater numbers than roots of DIMBOA-deficient lines. Although BX-dependent rhizosphere attraction of P. putida occurred in both autoclaved and non-autoclaved soil (Figure 5), the difference in P. putida colonisation between BX1 and bx1 lines in non-autoclaved soil was only consistent between both lines during the relatively young developmental stages of the plants (Figure 5B). This age-dependent decline in P. putida response to BXs concurs with our finding that DIMBOA root exudation declines steadily as seedlings age (Figure 1). In autoclaved soil, however, this age-dependency was unclear. Autoclaved soil provides a much less competitive environment for the introduced P. putida bacteria than non-autoclaved soil. It is, therefore, plausible that the lower exudation rates of DIMBOA from older plants are still sufficient to attract the bacteria from non- autoclaved soil to the rhizosphere. Alternatively, it is possible that HDMBOA-glc, which did not show a noticeable age-dependent decline in exudation rate (Figure 1), contributes to bacterial recruitment at later developmental stages of the host plant. In both autoclaved and non-autoclaved soil, numbers of other rhizosphere bacteria were similar between roots of BX1 and bx1 plants (Figure 5). The difference in response to BX-exuding roots between P. putida and other rhizobacteria indicates that the microbial composition of the rhizophere is strongly influenced by the presence of DIMBOA in root exudates of the host plant. Apart from direct anti-microbial effects, DIMBOA root exudation may have an additive effect considering that DIMBOA-exposed P. putida showed enhanced expression of the phzF gene (Table I), which encodes an enzyme in the biosynthesis of the broad-spectrum antibiotic phenazine (Blankenfeldt et al., 2004). Other studies have revealed bacterial attraction to 104
105 Recruitment of beneficial bacteria by maize roots primary metabolites in plant roots: L-leucine and L-malate attract P. fluorescens to tomato roots (De Weert et al., 2002), while L-malate was found to promote attraction of Bacillus subtilis to the rhizosphere of Arabidopsis thaliana (De Weert et al., 2002). To our knowledge, DIMBOA is the first allelochemical shown to act as a chemo-attractant for beneficial rhizobacteria, which may explain why P. putida KT2440 is such a successful coloniser of the maize rhizosphere (Molina et al., 2000). Our discovery also strengthens the notion that certain bacteria have acquired the ability to detoxify aromatic plant compounds, allowing them to exploit the energy-rich rhizosphere of plant roots exuding allelochemical compounds. These same bacteria can be exploited for the remediation of aromatic pollutants and herbicides (Parales and Harwood, 2002). In summary, our study has shown that root exudation of BXs attracts plant beneficial rhizobacteria. Although BX biosynthesis is mostly developmentally regulated (Frey et al., 2009), recent evidence has revealed that BX production by maize seedlings is to a certain extent responsive to environmental stimuli (Erb et al., 2009; Erb et al., 2009). It would, therefore, be interesting to examine the BX-dependent effects on rhizobacteria during adaptive interactions between above- and belowground defences. Our study also provides important knowledge for agricultural programmes aiming at sustainable yield improvement of cereal crops. Management of soil-borne diseases has proved problematic, because plant roots are relatively inaccessible for fungicidal chemicals. Furthermore, growth promotion by excessive soil fertilisation can have detrimental environmental impacts. Selection for cereal varieties with an increased capacity for BX root exudation will lead to crops with an improved ability to recruit disease-suppressive and growth-promoting rhizosphere communities, thereby reducing the need for repeated applications of fungicides and fertilisers. However, there is evidence that the specialist Western Corn Rootworm (Diabrotica virgifera) uses root-exuded BXs, such as DIMBOA and MBOA, as feeding cues (Bjostad and Hibbard, 1992; Robert et al., 2012). The potential for crop improvement by selection for increased BX exudation should therefore be approached with caution. On the other hand, the accelerated degradation of DIMBOA and MBOA by P. putida (Figure 2B) may interfere with host location by D. virgifera and pose a potential opportunity for biocontrol of this pest. ACKNOWLEDGEMENTS We thank Prof. Dieter Sicker, University of Leipzig, Germany, for providing us with various standards of BX compounds and Dr. Arnaud Dechesne, Technical University of Denmark, Lyngby for providing the GFP-tagged strain, FBC004. We would also like to thank two anonymous reviewers for their constructive comments on the original version of the manuscript, which helped to improve the manuscript greatly. None of the authors declare any conflicts of interest.
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Plant basal resistance: genetics, b
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Most of the research described in t
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Promotor: Prof. dr. Ir. C.M.J. Piet
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10 CHAPTER 1 General Introduction A
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Chapter 1 (PRRs; Gomez-Gomez and Bo
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Chapter 1 by avirulent pathogens (R
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Chapter 1 Selective non-pathogenic
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Chapter 1 an endogenous plant signa
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Chapter 1 between defence signallin
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Chapter 1 rarely provides complete
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Chapter 1 genetic resources for Ara
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Chapter 1 metabolites are biosynthe
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Chapter 1 constitutively produced i
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Chapter 1 latest insights. This Cha
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ABSTRACT 33 Genetic dissection of b
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35 Genetic dissection of basal defe
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Natural variation in responsiveness
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Page 53 and 54: 53 Genetic dissection of basal defe
Page 55 and 56: 55 Genetic dissection of basal defe
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Page 61 and 62: ABSTRACT 61 Role of benzoxazinoids
Page 63 and 64: 63 Role of benzoxazinoids in maize
Page 67 and 68: Chemical treatments and callose qua
Page 69 and 70: Aphid infestation stimulates apopla
Page 81 and 82: Table S1: Primers used for RT-qPCR
Page 86 and 87: 86 CHAPTER 4 Benzoxazinoids in root
Page 88 and 89: Chapter 4 INTRODUCTION Plants have
Page 90 and 91: Chapter 4 Our study presents eviden
Page 92 and 93: Chapter 4 Maize - P. putida FBC004
Page 94 and 95: Chapter 4 P. putida is tolerant to
Page 96 and 97: Chapter 4 Impact of DIMBOA on the P
Page 98 and 99: Chapter 4 PP5286 dut deoxyuridine 5
Page 100 and 101: Chapter 4 DIMBOA-producing wild-typ
Page 102 and 103: Chapter 4 DISCUSSION The rhizospher
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Page 108 and 109: 108 CHAPTER 5 General Discussion
Page 110 and 111: Chapter 5 QTL was caused by a polym
Page 112 and 113: Chapter 5 Figure 1: CYP81D11 regula
Page 114 and 115: Chapter 5 et al., 2009), and allele
Page 116 and 117: Chapter 5 defence against different
Page 118 and 119: Chapter 5 occurred at time-points l
Page 120 and 121: Chapter 5 rhizospheric signals that
Page 122 and 123: Chapter 5 glucosinolate profiles. 1
Page 124 and 125: References References Abramovitch R
Page 126 and 127: References QTL mapping and characte
Page 128 and 129: References Gianoli E, Niemeyer HM (
Page 130 and 131: References Kliebenstein DJ, Kroyman
Page 132 and 133: References Studies in Natural Produ
Page 134 and 135: References Geniostoma antherotrichu
Page 136 and 137: References Todesco M, Balasubramani
Page 138 and 139: References Walters DR, Paterson L,
Page 140 and 141: Summary Summary Basal resistance in
Page 142 and 143: Samenvatting Samenvatting Basale re
Page 144 and 145: Samenvatting inzichten opgeleverd i
Page 146 and 147: Acknowledgments Acknowledgements In
Page 148 and 149: Curriculum vitae Shakoor was born o
Page 150: List of Publications Published arti
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