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Evaluating the Efficacy of Plant Growth Promoting Rhizobacteria in Australian Agriculture

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Evaluating the Efficacy of Plant Growth Promoting Rhizobacteria in Australian Agriculture Evaluating the Efficacy of Plant Growth Promoting Rhizobacteria In Australian Agriculture Shelby Kathleen Berg Bachelor of Science (Hns) A thesis submitted for the degree of Doctor of Philosophy at The University of Queensland in 2021 School of Agriculture and Food Sciences Abstract Interest in the soil edaphon is rising with the appreciation that soil biological processes are a main contributor of planetary and ecosystem function, and agricultural productivity. Soils under agricultural production often accumulate crop pathogens, while crop-beneficial microbes may be present in insufficient numbers. An attractive concept is engineering microbial communities to improve crop resilience, development, growth and yield. Plant growth promoting rhizobacteria (PGPR) and other beneficial microbes that improve plant and soil function (termed ‘biostimulants’ in the following) could lower the costs for farmers and the environment. While some countries require manufacturers to provide proof-of-efficacy, the sector remains largely unregulated, including in Australia. There is doubt about the efficacy of many biostimulants because crop relevant scientific evaluations are mostly not in the public domain. As it stands, it has been argued that research has to advance knowledge of plant-microbe-soil interactions to identify suitable strategies for enabling effective biostimulants. The overarching aim of this thesis was to evaluate putative PGPR and soil-enhancing microbes across several levels of experimental control to advance this knowledge frontier for tropical crops. Two chapters (Chapters 2 and 3) report on experiments that tested putative (i) commercial biostimulants and soil enhancing products Soil-LifeTM and Nutri-Life Platform® in a sugarcane field in Queensland’s wet tropics, and (ii) PGPR Serenade® Prime, Rhizo-max, Great Land® and an isolate of Enterobacter at a commercial seedling nursery and in controlled growth cabinets. The effects of microbial inoculation were evaluated with growth and physiological responses, and with phylogenetic marker gene sequencing to analyse microbial communities in root+rhizosphere (‘root’ in the following) and soil. Microbial inoculation did not enhance yield (sugarcane crop) or growth (seedlings of watermelon, tomato, pumpkin), and Great Land®-inoculated watermelon seedlings had significantly less biomass than the un-inoculated control. In field-grown sugarcane, root and soil bacterial communities were unaffected by commercial biostimulants. However, root fungal communities showed a significant increase of Fusarium, Marasmius and Talaromyces populations, confirming that inoculation can indirectly alter microbial communities, but evaluating whether this change convey benefits was beyond scope. Microbial communities of nursery-grown seedlings were not analysed. Instead, we tested sugarcane and watermelon seedlings under well-watered and water limited (stressed) conditions to determine if inoculation with active or inactive microbes conveys benefits. Inoculation did not affect the growth of well-watered seedlings. Water-stressed seedlings grew significantly less than non-stressed seedlings, an exception were watermelon seedlings inoculated with active Rhizo-max which produced similar biomass as well-watered seedlings. Root communities of water-stressed and inoculated seedlings had altered bacterial community composition and species richness. Similar to the field experiment, taxa present in the inoculants did Page 2 of 167 not form the dominant genera of the root communities or increase in relative abundance. Taken together, the findings show that commercial microbial products are mostly ineffective in the test systems. A third chapter (Chapter 4) reports on the screening of PGP traits of 121 culturable bacterial isolates that originated from the roots of non-inoculated field-grown sugarcane. We tested the in vitro expression of PGP traits, which often informs the selection for biostimulant products, to gain insight of trait distribution and efficacy. Sanger sequencing identified as dominant genera Serratia (43%, Enterobacteriaceae), Pseudomonas (20%, Pseudomonadaceae) and Bacillus (18%, Bacillaceae). These taxa encompass species that have been identified as PGPR previously. Screening 10 PGP traits in vitro showed that the isolates could be broadly categorised into two groups. The first group expressed one or two PGP traits to a high level, the second expressed three or more PGP traits to low or moderate levels, so that the isolates could be broadly classified into ‘specialists’ and ‘generalists’. We then tested whether in vitro activity translates to in vivo effectiveness using bioassays. The first assay used IPT-mutant Arabidopsis to evaluate cytokinin producing bacteria. Of the three cytokinin producers tested, only two affected plant growth either by producing cytokinin or affecting the cytokinin biosynthesis pathway. The second assay involved five isolates with the highest biocontrol activity in vitro and Gummy Stem Blight (GSB, Stagonosporopsis), a fungal disease of Curcurbitaceae. All isolates resulted in somewhat reduced GSB disease severity in watermelon seedlings, including a Bacillus isolate that extensively colonised fungal hyphae on the leaf surface. These findings are promising and have to be furthered to develop PGPR as an effective tool in plant production. We propose that the current focus on selecting PGPR based on in vitro tests should be expanded to screening effective root colonisation to ensure a strong ability to establish with and colonise target crops. Whether ‘specialist’ or ‘generalist’ PGPR hold promise for product development should be investigated. We discuss effective microbe delivery and the implications of inducible PGP traits on microbial survival. Taken together, the research confirms the need for improved products and their delivery, which will likely include more specific uses of optimised biostimulants for particular species and settings. It confirms that current products can affect root microbial communities, and in one instance, show efficacy. While regulators are reining in the rapidly expanding biostimulant market in some regions by demanding evidence of efficacy, similar action is needed for tropical crops. Ideally, R&D should be performed in industry relevant settings and underpinned by fundamental research on the behaviour of microbes in soil and root communities. Collaboration between government regulators, biostimulant producers, crop industries and independent research agencies is required to deliver the promise of green agriculture; in Chapter 5, we discuss the way forward. Page 3 of 167 Declaration by author This thesis is composed of my original work, and contains no material previously published or written by another person except where due reference has been made in the text. I have clearly stated the contribution by others to jointly-authored works that I have included in my thesis. I have clearly stated the contribution of others to my thesis as a whole, including statistical assistance, survey design, data analysis, significant technical procedures, professional editorial advice, financial support and any other original research work used or reported in my thesis. The content of my thesis is the result of work I have carried out since the commencement of my higher degree by research candidature and does not include a substantial part of work that has been submitted to qualify for the award of any other degree or diploma in any university or other tertiary institution. I have clearly stated which parts of my thesis, if any, have been submitted to qualify for another award. I acknowledge that an electronic copy of my thesis must be lodged with the University Library and, subject to the policy and procedures of The University of Queensland, the thesis be made available for research and study in accordance with the Copyright Act 1968 unless a period of embargo has been approved by the Dean of the Graduate School. I acknowledge that copyright of all material contained in my thesis resides with the copyright holder(s) of that material. Where appropriate I have obtained copyright permission from the copyright holder to reproduce material in this thesis and have sought permission from co-authors for any jointly authored works included in the thesis. Page 4 of 167 Publications during candidature Berg S, Dennis PG, Paungfoo‐Lonhienne C, et al (2020) Effects of commercial microbial biostimulants on soil and root microbial communities and sugarcane yield. Biol Fertil Soils 56:565– 580 Publications included in this thesis Berg S, Dennis PG, Paungfoo‐Lonhienne C, et al (2020) Effects of commercial microbial biostimulants on soil and root microbial communities and sugarcane yield. Biol Fertil Soils 56:565– 580 Manuscripts included in this thesis Chapter Two Berg S, Dennis PG, Paungfoo‐Lonhienne C, et al (2020) Effects of commercial microbial biostimulants on soil and root microbial communities and sugarcane yield. Biol Fertil Soils 56:565– 580 Chapter Three Berg S, Dennis PG, Schmidt S, et al (2021) Examining the efficacy of commercial PGPR products for seedling production in horticulture. unpublished Chapter Four Berg S, Dennis PG, Schmidt S, et al (2021) Screening rhizobacteria for plant growth promoting traits. unpublished Contributor Statement of contribution Shelby Berg Conception and design (10%) Analysis and interpretation (55%) Drafting and production (60%) Susanne Schmidt Conception and design (40%) Analysis and interpretation (10%) Drafting and production
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