Antagonistic Plants Preferentially Target Arbuscular Mycorrhizal Fungi That Are Highly 4 Connected to Mutualistic Plants
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No reuse allowed without permission. 1 FULL PAPER 2 3 Antagonistic plants preferentially target arbuscular mycorrhizal fungi that are highly 4 connected to mutualistic plants 5 6 Sofia IF Gomes1, Miguel A Fortuna2, Jordi BasCompte2, VinCent SFT MerCkx3,4* 7 8 9 1 Institute of Biology, Leiden University, Leiden, the Netherlands 10 2 Department of Evolutionary Biology and Environmental Studies, University of ZuriCh, 11 Switzerland. 12 4 Naturalis Biodiversity Center, Leiden, the Netherlands 13 3 Department of Evolutionary and Population Biology, Institute for Biodiversity and ECosystem 14 DynamiCs, University of Amsterdam, Amsterdam, the Netherlands 15 16 * Corresponding author: [email protected] 1 bioRxiv preprint doi: https://doi.org/10.1101/867259; this version posted July 5, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 17 Summary 18 19 • How antagonists – myCoheterotrophiC plants that obtain Carbon and soil nutrients from 20 fungi – are integrated in the usually mutualistiC arbusCular myCorrhizal networks is 21 unknown. Here, we Compare mutualistiC and antagonistiC plant assoCiations with 22 arbusCular myCorrhizal fungi and use network analysis to investigate fungal assoCiation 23 preferences in the tripartite network. 24 • We sequenced root tips from mutualistiC and antagonistiC plants in a tropiCal forest to 25 assemble the Combined tripartite network between mutualistiC plants, myCorrhizal fungi, 26 and antagonistiC plants. We Compared the fungal eCologiCal similarity between 27 mutualistiC and antagonist networks, and searChed for modules (an antagonistiC and a 28 mutualistiC plant interacting with the same pair of fungi) to investigate whether pairs of 29 fungi simultaneously linked to plant speCies from each interaction type were 30 overrepresented throughout the network. 31 • AntagonistiC plants interacted with approximately half the fungi deteCted in mutualistiC 32 plants. Antagonists were indireCtly linked to any of the deteCted mutualistiC plants, and 33 fungal pairwise eCologiCal distanCes were Correlated in both network types. Moreover, 34 pairs of fungi sharing the same antagonistiC and mutualistiC plant speCies oCCurred more 35 often than expeCted by ChanCe. 36 • We hypothesize that the maintenanCe of antagonistiC interactions is maximized by 37 targeting well-linked mutualistiC fungi, thereby minimizing the risk of Carbon supply 38 shortages. 39 40 Keywords: myCoheterotrophy, myCorrhizal networks, arbusCular myCorrhizal fungi, 41 antagonism, mutualism 2 bioRxiv preprint doi: https://doi.org/10.1101/867259; this version posted July 5, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 42 Introduction 43 SinCe the early history of life, interspeCifiC mutualisms have been paramount in the 44 funCtioning of eCosystems (Thompson, 2005; BasCompte & Jordano, 2013). Mutualisms Can 45 form Complex networks of interdependenCe between dozens or even hundreds of species. A 46 prime example of this ‘web of life’ is the 450-million-year-old mutualism between the 47 majority of land plants and arbusCular myCorrhizal (AM) fungi (Strullu-Derrien et al., 2018). In 48 this interaction plants supply the arbusCular myCorrhizal GlomeromyCotina and 49 MuCoromyCotina fungi with Carbohydrates, essential for fungal survival and growth. In return, 50 the fungi provide their host plants with mineral nutrients and water from the soil (Smith & 51 Read, 2008; Bidartondo et al., 2011). One of the key CharacteristiCs of the arbusCular 52 myCorrhizal interaction is its low interaction speCifiCity: a myCorrhizal plant typiCally 53 assoCiates simultaneously with multiple fungi and a myCorrhizal fungus often assoCiates 54 simultaneously with multiple plants (Lee et al., 2013). This Creates Complex underground 55 networks in whiCh plants of different speCies are indireCtly linked through shared arbusCular 56 myCorrhizal fungi (Toju et al., 2015; Chen et al., 2017). Despite this low speCifiCity, there is 57 evidenCe that networks of plants and arbusCular myCorrhizal fungi do not assemble randomly, 58 and effeCts of plant funCtional group (Davison et al. 2011; Sepp et al., 2019), and plant or 59 fungal evolutionary relationships (Montesinos-Navarro et al., 2015; Chen et al., 2017) on 60 arbusCular myCorrhizal interaction networks have been reported. 61 62 Considerable progress has been made in disseCting the exChange of resourCes between plants 63 and AM fungi, and its regulation, in reCent years. Experimental work on low-diversity systems 64 has demonstrated that Control is bidireCtional, and partners offering the best rate of 65 exChange are rewarded, suggesting that AM networks Consist of ‘fair trade’ interactions 66 (Bever et al., 2009; Kiers et al., 2011). However, the importanCe of reCiproCally regulated 67 resource exChange is questioned, as myCorrhizas also affeCt plant health, interactions with 68 other soil organisms, host-defense reactions, and suppression of non-myCorrhizal Competitor 69 plants (Walder & Van Der Heijden, 2015). Also, striCtly reCiproCal regulation of resourCe 70 exChange does not seem to apply to all AM interactions. Some exCeptional plants, for 71 example, behave as antagonists (Selosse & Rousset, 2011; Walder & Van Der Heijden, 2015): 72 myCoheterotrophiC plants Can obtain Carbon from root-assoCiated fungi and some speCies 3 bioRxiv preprint doi: https://doi.org/10.1101/867259; this version posted July 5, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 73 have replaced photosynthesis by Carbon uptake from arbusCular myCorrhizal fungi (Leake, 74 1994; MerCkx, 2013). The meChanism underpinning Carbon transfer from arbusCular 75 myCorrhizal fungi to myCoheterotrophiC plants remains unClear, but it is unlikely that resourCe 76 exChange in these myCoheterotrophiC assoCiations relies on reCiproCal dynamiCs. HenCe, 77 myCoheterotrophiC plants are Considered Cheaters of the myCorrhizal symbiosis beCause they 78 exploit the arbusCular myCorrhizal symbiosis for soil nutrients and Carbon without 79 reCiproCating, to our Current knowledge (Selosse & Rousset, 2011), or without apparently 80 being sanCtioned by the fungal partners (Walder & Van Der Heijden, 2015). Moreover, it has 81 been suggested that myCoheterotrophiC plants may display a truly biotrophiC parasitiC mode, 82 digesting the fungus Colonizing their roots (Imhof et al., 2013). 83 84 PhylogenetiC studies demonstrate that these Cheaters evolved from mutualistiC anCestors 85 (MerCkx et al., 2013). Within obligate mutualisms, the CritiCal barrier to mutualism breakdown 86 and to the evolutionary stability of the resulting Cheater speCies is thought to be a 87 requirement for three-speCies CoexistenCe: a Cheater plant relies on a mutualistiC partner – a 88 myCorrhizal fungus – which simultaneously interacts with a mutualistiC plant (Pellmyr & 89 Leebens-Mack, 1999). In species-rich mutualisms suCh as the arbusCular myCorrhizal 90 symbiosis, where multi-speCies CoexistenCe is the rule, a high potential for the oCCurrenCe of 91 these tripartite linkages is expeCted (MerCkx & Bidartondo, 2008). Indeed, while evolution of 92 Cheating in speCialized obligate mutualisms is relatively rare (Sachs & Simms, 2006), Cheating 93 in the arbusCular myCorrhizal symbiosis evolved in more than a dozen of plant Clades, 94 including over 250 species whiCh together occur in nearly all tropiCal and subtropiCal forests 95 (MerCkx, 2013; Gomes et al., 2019a). 96 97 Previous work has shown that myCoheterotrophiC plants – hereafter ‘antagonists’ – target a 98 subset of the myCorrhizal fungi available in the loCal Community (e.g Bidartondo et al. (2002); 99 Gomes et al. (2017a); Sheldrake et al. (2017)). Their assoCiated fungal Communities Can vary 100 in speCifiCity (MerCkx et al., 2012), and in Communities of Co-occurring antagonists the 101 phylogenetiC diversity of their fungal assoCiations appears to inCrease proportionally to their 102 fungal overlap, a pattern whiCh potentially responds to an eCologiCal meChanism driven by 103 maximizing Co-oCCurrenCe and avoiding Competitive exClusion among antagonistiC plants. 4 bioRxiv preprint doi: https://doi.org/10.1101/867259; this version posted July 5, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 104 (Gomes et al., 2017b). However, whether partner ChoiCe of these antagonists is affeCted by 105 mutualistiC myCorrhizal interactions is Currently unknown. Here, we hypothesize that 106 antagonists preferentially assoCiate with ‘keystone’ (Mills & Doak, 1993) fungi that are 107 ConneCted to many different mutualistiC plants, sinCe these fungi are potentially more 108 resilient to perturbations (BasCompte & Jordano, 2007) and may be the most reliable sourCe 109 of Carbon (Waterman et al., 2013). In addition, sinCe fungal traits play an important role in 110 arbusCular myCorrhizal interactions – phylogenetiCally related AM fungi (assumed to have 111 similar funCtional