The Ability of Plants to Produce Strigolactones Affects Rhizosphere Community Composition of Fungi but Not Bacteria

Author’s Accepted Manuscript The ability of plants to produce strigolactones affects rhizosphere community composition of fungi but not bacteria Lilia Costa Carvalhais, Vivian A. Rincon-Florez, Philip B. Brewer, Christine A. Beveridge, Paul G. Dennis, Peer M. Schenk www.elsevier.com PII: S2452-2198(18)30116-2 DOI: https://doi.org/10.1016/j.rhisph.2018.10.002 Reference: RHISPH128 To appear in: Rhizosphere Received date: 23 September 2018 Revised date: 23 October 2018 Accepted date: 23 October 2018 Cite this article as: Lilia Costa Carvalhais, Vivian A. Rincon-Florez, Philip B. Brewer, Christine A. Beveridge, Paul G. Dennis and Peer M. Schenk, The ability of plants to produce strigolactones affects rhizosphere community composition of fungi but not bacteria, Rhizosphere, https://doi.org/10.1016/j.rhisph.2018.10.002 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting galley proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. The ability of plants to produce strigolactones affects rhizosphere community composition of fungi but not bacteria Lilia Costa Carvalhais1,2*, Vivian A. Rincon-Florez1,2, Philip B. Brewer3, Christine A. Beveridge3, Paul G. Dennis4, Peer M. Schenk1 1School of Agriculture and Food Sciences, The University of Queensland, Brisbane, QLD 4072, Australia; 2Centre for Horticultural Science, Queensland Alliance for Agriculture Food and Innovation, Ecosciences Precinct, Dutton Park, 4001, Australia; 3School of Biological Sciences, The University of Queensland, Brisbane, QLD 4072, Australia; and 4School of Earth and Environmental Sciences, The University of Queensland, Brisbane, QLD 4072, Australia *Corresponding author: [email protected] Abstract Strigolactones are an important group of plant hormones. When released from roots, they act as signalling molecules that induce branching of arbuscular mycorrhizal hyphae. However, the extent to which they affect the rhizosphere microbiome is unknown. Filling this knowledge gap is important because the diversity and composition of the root-associated microbiome influence plant fitness. In this study, we hypothesised that strigolactone- producing plants harbour a different community of rhizosphere bacteria and fungi compared to plants whose strigolactone synthesis is impaired. To test this hypothesis, we compared the diversity of rhizosphere bacterial and fungal communities associated with wild-type Arabidopsis thaliana and a mutant impaired in the production of strigolactones due to a disruption of the MORE AXILLARY GROWTH 4 (MAX4) gene. Our results indicate that the plant’s ability to produce strigolactone is significantly correlated with changes in the composition (beta diversity) of rhizosphere fungal but not bacterial communities. No differences in alpha diversity (richness and evenness) were observed for either bacterial or fungal communities between the rhizospheres of max4 and wild-type. Epicoccum nigrum, Penicillium, Fibulochlamys chilensis, Herpotrichiellaceae, Mycosphaerella and Mycosphaerellaceae were among the fungal taxa possibly attracted to or mostly influenced by strigolactones given that they were present at higher abundances in the rhizosphere of the wild-type compared to the mutant. Our study provides evidence that rhizosphere fungal diversity are more strongly affected than bacterial diversity by the plant’s ability to produce strigolactones. Keywords: terpenoid lactones, strigolactones, phytohormones, fungi, bacteria, rhizosphere, diversity Introduction Plants are sessile organisms that use a wide-range of signalling molecules to interact with other organisms and coordinate responses to environmental changes. For instance, root- released compounds can influence soil-microbe composition and soil microbes can have a promotive effect on plant growth (Carvalhais et al., 2015; Sasse et al., 2018). However, the extent to which plants interact with and derive various benefits from soil microbes may be broader than previously thought. To test this hypothesis further, we used a non-mycorrhizal plant species to explore the impact of strigolactones exuded from plant roots on the diversity of the rhizosphere microbiome. Strigolactones are carotenoid-derived molecules that play important roles in the regulation of plant development and chemical communication during biotic interactions (Brewer et al., 2013; Smith, 2014). While their first discovered role was to induce seed germination of parasitic plants (Cook et al., 1966), it was later found that they initiate and trigger symbiotic interactions between plants and arbuscular mycorrhizal fungi – AMF (Akiyama et al., 2005; Parniske, 2008). The mutual relationship between AMF occurs with c. 80% of land plants and date from approx. 450 million years ago (Parniske, 2008). Strigolactones have been linked to nodule initiation and rhizobacterial swarming in legumes, and interactions with bacterial, fungal and oomycetes pathogens (Akiyama and Hayashi, 2006; McAdam et al., 2017). These findings suggest that the diversity of plant-microbe interactions mediated by strigolactones is much more extensive than previously appreciated. Functions of strigolactones in symbiotic interactions have been mostly reported for plants and AMF. When secreted by roots, these compounds not only trigger AMF hyphal branching during the pre-symbiotic stage, but also induce spore germination and metabolism (Besserer et al., 2006; Mori et al., 2016). The hyphal network of AMF outreaches the rhizosphere, accesses nutrients and water from a greater volume of soil, and transfers these nutrients to the roots in exchange of photosynthates (Smith and Read, 2010; Yoneyama et al., 2007a). This helps plants access nutrients like phosphorus, which have limited mobility in the soil (Yoneyama et al., 2007b). Indeed, depending on the species, strigolactone secretion from roots increases to enhance AMF symbiosis, particularly under phosphorus (P) deficiency (Yoneyama et al., 2012). Furthermore, AMF require a component of strigolactone signalling to penetrate into roots in rice and pea and, in the case of rice, the karrikin receptor complex is also needed for perception of AMF (Yoshida et al., 2012; Foo et al., 2013; ). In contrast, high exogenous phosphate supply systemically suppresses AM colonization and symbiotic gene expression (Breuillin et al., 2010). This may be a mechanism for plants to limit symbiosis with AMF unless nutrients are low. Nonetheless, comparative transcriptomic analysis in petunia, rice, Medicago and Lotus suggested that the repressed genes encode not only carotenoid and strigolactone biosynthesis, but also proteases and phosphate transporters (Breuillin et al., 2010). This suggests that strigolactones do not solely regulate P responses in plants. Moreover, pea mutants that were impaired in strigolactone biosynthesis and sensing were poorly colonised by AM compared to the wild-type, which also indicates that phosphate supply is not the only factor controlling mycorrhizal symbiosis (Foo et al., 2013). Non-mycotrophic plants including Lupinus spp. (Yoneyama et al., 2008) and Arabidopsis thaliana (Goldwasser et al., 2008) also release strigolactones from roots, which indicates that these signals may be involved in processes other than the ones mediating mycorrhizal associations. For example, in legumes, strigolactones are involved in symbiosis with rhizobial bacteria. They enhance bacterial motility on surfaces, known as swarming, which facilitate the establishment of the interaction (Pelaez-Vico et al., 2016). Furthermore, endogenous strigolactones positively control nodulation of pea, alfalfa (Medicago sativa), Medicago truncatula, soybean (Glycine max) and Lotus japonicus (Foo and Davies, 2011; Liu et al., 2013; McAdam et al., 2017; Rehman et al., 2018; Soto et al., 2010; van Zeijl et al., 2015). It is also important to note that although canonical strigolactones have been reported in Arabidopsis root exudates (Goldwasser et al., 2008), these results were never confirmed with more modern analytical chemistry systems (Yoneyama et al., 2018). Non-canonical rather than canonical strigolactones have then been proposed to act more frequently as rhizosphere signals as they seem to be more common in root exudates of various plants (Yoneyama et al., 2018). The involvement of strigolactones in plant defence has also been reported (Marzec, 2016; Torres-Vera et al., 2014). Strigolactone-deficient tomato plants exhibited higher susceptibility to the necrotrophic fungi Botrytis cinerea and Alternaria alternata (Torres-Vera et al., 2014). However, when infected with the hemibiotrophic oomycete Pythium irregulare and fungus Fusarium oxysporum, strigolactone deficient pea showed no differences in susceptibility to disease compared with the wild-type (Abe et al., 2014; Blake et al., 2016). When using an in vitro system to examine the effect of the synthetic strigolactone GR24 on a range of phytopathogenic fungi, growth inhibition was observed for Fusarium oxysporum f. sp. melonis, Fusarium solani f. sp. mango, Sclerotinia sclerotiorum, Macrophomina phaseolina, Alternaria alternata, Colletotrichum acutatum and Botrytis cinerea; while intense branching was observed for S. sclerotiorum, C.

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