Comprehensive Analysis of the Apple Rhizobiome As Influenced by Different T Brassica Seed Meals and Rootstocks in the Same Soil/Plant System ⁎ Tracey S

Applied Soil Ecology 157 (2021) 103766 Contents lists available at ScienceDirect Applied Soil Ecology journal homepage: www.elsevier.com/locate/apsoil Comprehensive analysis of the apple rhizobiome as influenced by different T Brassica seed meals and rootstocks in the same soil/plant system ⁎ Tracey S. Someraa, , Shiri Freilichb, Mark Mazzolaa,c a United States Department of Agriculture-Agricultural Research Service Tree Fruit Research Lab, 1104 N. Western Ave., Wenatchee, WA 98801, United States of America b Agricultural Research Organization (ARO) and The Volcani Center, Institute of Plant Sciences, Ramat Yishay, Israel c Department of Plant Pathology, Stellenbosch University, Private Bag X1, Matieland 7600, South Africa ARTICLE INFO ABSTRACT Keywords: Replant disease refers to the poor growth of trees when attempting to establish the same or related species on old Apple replant disease orchard sites. The use of pre-plant Brassicaceae seed meal (SM) soil amendments in combination with apple Brassica replant disease-tolerant rootstock genotypes has been shown to be a promising strategy for the control of apple Rootstock genotype replant disease (ARD). However, optimizing microorganism-driven protection of apple roots from infection by Oomycete multiple soil-borne pathogens requires a more comprehensive understanding of how “effective” vs. “ineffective” Brassicaceae seed meal × rootstock genotype disease control systems modulate the composition of rhizosphere microbial communities. In particular, the community of oomycetes associated with the apple rhizosphere re- mains relatively unexplored compared with bacteria and fungi. To address these issues, we sequenced the root associated bacterial, fungal, and oomycete communities of apple replant disease tolerant (G.210) and susceptible (M.26) rootstocks when grown in an orchard replant soil amended with different Brassicaceae seed meal for- mulations (Brassica juncea + Sinapis alba, B. juncea, and Brassica napus) previously shown to provide varying levels of replant disease control. Multiple microbial components were associated with observed growth differ- ences between “effective” and “ineffective” disease control systems including the absolute abundance of Ilyonectria/Cylindrocarpon in fine root tissue. Amplicon sequencing provided a more detailed picture ofthege- netic diversity of oomycete groups in the apple rhizosphere than previously appreciated, and highlighted the variability in oomycete community structure between different rootstock × seed meal disease control systems. In Brassica juncea + Sinapis alba SM-structured rhizospheres, the ARD-tolerant rootstock (G.210) harbored higher relative abundances of Peronosporales with reduced potential to infect apple roots and incite replant disease (such as Peronospora destructor and P. acanthicum), whereas the Peronosporales community associated with the sensitive rootstock (M.26) was dominated by the ARD-specific pathogen Phytophthora cactorum. In addition, Brassica juncea + Sinapis alba SM-structured microbiomes were characterized by numerous bacterial and fungal taxa with the potential for biocontrol, biodegradation and bioremediation. Taken together, these results support the hypothesis that particular Brassicaceae SM soil amendments not only provide “effective” disease control, but also promote microbiomes which are likely to contribute to long-term orchard soil health in many other ways. Overall, this comprehensive analysis highlights the significance of the rootstock × seed meal interaction on bacterial, fungal, and oomycete communities within the apple rhizosphere of “effective” vs. “ineffective” disease control systems and the potential influence of these elements on the dynamics ofapple replant disease. 1. Introduction disease (ARD) is primarily due to plant-induced changes in the soil microbiota leading to a build-up of multiple soil-borne pathogens over Replant disease refers to the poor growth of trees when attempting time. In many apple-growing regions of the world, including South to establish the same or related species on old orchard sites (replant Africa, Italy, Australia, New York and Washington State, the causative sites) and is known to largely affect nut as well as stone and pome fruit agents of the disease complex typically include the root lesion nema- trees, including many members of the Rosaceae family. Apple replant tode Pratylenchus spp. in addition to multiple root-associated fungal ⁎ Corresponding author. E-mail address: [email protected] (T.S. Somera). https://doi.org/10.1016/j.apsoil.2020.103766 Received 29 June 2020; Received in revised form 25 August 2020; Accepted 27 August 2020 Available online 18 September 2020 0929-1393/ © 2020 Published by Elsevier B.V. T.S. Somera, et al. Applied Soil Ecology 157 (2021) 103766 (Rhizoctonia solani, Ilyonectria/Cylindrocarpon) and oomycete (Pythium, activity of isothiocyanates. Brassicaceae seed meals are complex carbon Phytophthora) pathogens (Dullahide et al., 1994; Manici et al., 2013; substrates that require specific metabolic pathways for effective utili- Mazzola, 1998; Tewoldemedhin et al., 2011a, 2011b). Economic losses zation. As a result of these two features, the BjSa SM formulation results due to reduced tree growth and survival during the first four years of in transformation of the fungal and bacterial rhizosphere communities orchard replanting can run anywhere from US$40,000–$150,000 per and ultimately possesses functional features providing long-term con- acre over a 10-year period (Hewavitharana et al., 2019). Widespread trol of ARD pathogens (Mazzola et al., 2015; Wang and Mazzola, 2019a, use of soil fumigation in Washington State using broad-spectrum che- 2019b; Weerakoon et al., 2012). In field studies, BjSa SM-induced micals (e.g. methyl bromide) as a replant management strategy began modifications to the rhizosphere microbiome persisted over multiple in the early 1990s (Willett et al., 1994). During the last few decades growing seasons and were associated with prolonged pathogen sup- however, global efforts to phase-out methyl bromide (Schafer, 1999) pression (Mazzola et al., 2015; Wang and Mazzola, 2019a). and more recent regulatory actions to limit use of other fumigants (e.g. Integration of seed meal treatments with specific rootstock geno- 1,3-dichloropropene, chloropicrin) have reduced the economic or types known to possess ARD tolerance may be integral to the devel- practical long-term viability of utilizing this method for control of soil- opment of alternative ARD management strategies (Wang and Mazzola, borne pests and pathogens in certain geographic regions. In addition, 2019a). In general, apple rootstocks from the Geneva series have sup- such an approach is not compatible with the expanding production of ported lower populations of Pythium spp. and P. penetrans than Malling organic tree fruits in response to the increasing consumer demand, series rootstocks (Isutsa and Merwin, 2000; Mazzola, 2009; Wang and particularly in Europe and North America. One promising alternative Mazzola, 2019a, 2019b). The rootstock G.210 was specifically bred for strategy to chemical fumigation, suitable for use in conventional and resistance to crown and root rot caused by Phytophthora cactorum organic production systems, is the use of pre-plant Brassicaceae seed (Cummins et al., 2013). In a recent transcriptome study, when chal- meal (SM) soil amendments in combination with apple replant disease lenged with Pythium ultimum, host defense responses were initiated (ARD)-tolerant rootstock genotypes. These types of “effective” disease faster and stronger in the ARD-tolerant rootstock G.935 than in the control systems have repeatedly been shown to provide increased plant susceptible rootstock Bud.9 (Zhu et al., 2016). Another important as- productivity at or above the level attained through the traditional pect of ARD-tolerance is the finding that the tolerant rootstock G.210 practice of soil fumigation (Mazzola, 2009; Mazzola et al., 2015; Wang develops a more extensive fine-root system that is more readily shed and Mazzola, 2019a). and regenerated than in the susceptible rootstock M.26 (Atucha et al., Members of the Brassicaceae family produce an array of glucosino- 2014; Emmett et al., 2014). late compounds which vary both qualitatively and quantitatively by Root exudates which vary in a genotype-dependent manner also species and even by plant cultivar (Brown and Morra, 1997). In re- influence the structure and function of rhizosphere microbial commu- sponse to tissue disruption, and in the presence of water, glucosinolates nities (Leisso et al., 2018). The microorganisms immediately sur- are hydrolyzed by the enzyme myrosinase to result in multiple che- rounding the root play important roles in the growth and ecological mistries, including isothiocyanates, with potential to inhibit various fitness of their plant host. Although soil type has been reported tobea plant pathogenic organisms. Glucosinolates are present in highest major factor determining composition of rhizosphere fungal and bac- concentration in the seed (Popova and Morra, 2014) and thus, the seed terial communities (Chang et al., 2019; Qin et al., 2019; Singh et al., meal generated during the oil extraction process are a superior mate- 2007), the ability of SM amendments to enrich for microbial groups rial, relative to Brassicaceae green manures, as a soil amendment em- with activity against known ARD pathogens has been documented in ployed for the control of soil-borne

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