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Weeds Hosting the Soybean Cyst Nematode (Heterodera Glycines Ichinohe): Management Implications in Agroecological Systems

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Weeds Hosting the Soybean Cyst Nematode (Heterodera Glycines Ichinohe): Management Implications in Agroecological Systems agronomy Review Weeds Hosting the Soybean Cyst Nematode (Heterodera glycines Ichinohe): Management Implications in Agroecological Systems Leonardo F. Rocha * , Karla L. Gage, Mirian F. Pimentel , Jason P. Bond and Ahmad M. Fakhoury School of Agricultural Sciences, Southern Illinois University, Carbondale, IL 62901, USA; [email protected] (K.L.G.); [email protected] (M.F.P.); [email protected] (J.P.B.); [email protected] (A.M.F.) * Correspondence: [email protected] Abstract: The soybean cyst nematode (SCN; Heterodera glycines Ichinohe) is a major soybean-yield- limiting soil-borne pathogen, especially in the Midwestern US. Weed management is recommended for SCN integrated management, since some weed species have been reported to be hosts for SCN. The increase in the occurrence of resistance to herbicides complicates weed management and may further direct ecological–evolutionary (eco–evo) feedbacks in plant–pathogen complexes, including interactions between host plants and SCN. In this review, we summarize weed species reported to be hosts of SCN in the US and outline potential weed–SCN management interactions. Plants from 23 families have been reported to host SCN, with Fabaceae including most host species. Out of 116 weeds hosts, 14 species have known herbicide-resistant biotypes to 8 herbicide sites of action. Factors influencing the ability of weeds to host SCN are environmental and edaphic conditions, SCN initial inoculum, weed population levels, and variations in susceptibility of weed biotypes to SCN within a population. The association of SCN on weeds with relatively little fitness cost incurred by the latter may decrease the competitive ability of the crop and increase weed reproduction when SCN is present, feeding back into the probability of selecting for herbicide-resistant weed biotypes. Therefore, proper management of weed hosts of SCN should be a focus of integrated pest management (IPM) strategies to prevent further eco–evo feedbacks in the cropping system. Citation: Rocha, L.F.; Gage, K.L.; Pimentel, M.F.; Bond, J.P.; Fakhoury, A.M. Weeds Hosting the Soybean Keywords: Amaranthus tuberculatus; AMATA; Conyza canadensis; ERICA; eco–evo; herbicide resis- Cyst Nematode (Heterodera glycines tance; integrated pest management; IPM; integrated weed management; IWM; Lamium purpurem; Ichinohe): Management Implications LAMPU; Lamium amplexicaule; LAMAM; SCN management; soybean diseases in Agroecological Systems. Agronomy 2021, 11, 146. https://doi.org/ 10.3390/agronomy11010146 1. Introduction Received: 21 December 2020 Ecology and evolution may interact resulting in environmental changes, which then Accepted: 9 January 2021 feeds back into ecological relationships and species evolution to alter community assembly Published: 14 January 2021 and ecosystem function [1]. In fact, the plant–pathogen–herbicide complex may be a prime example of eco–evolutionary (eco–evo) feedback in agricultural systems. Herbicides Publisher’s Note: MDPI stays neu- can be agents of eco–evo dynamics, causing shifts in weed community composition and tral with regard to jurisdictional clai- ms in published maps and institutio- influencing weed–pathogen co-evolution [2]. Thus, animals and microbes which rely on nal affiliations. plants may be directly impacted by herbicides and will be driven to evolve in concert with their plant hosts in response to management [3]. Direct and indirect effects impact species evolution and eco–evo feedbacks within the environment [4,5]. The concept that herbicides may influence eco–evo feedbacks in agricultural systems, and specifically in the Copyright: © 2021 by the authors. Li- plant–pathogen–herbicide complex, is relatively novel, and there is definitely a need to censee MDPI, Basel, Switzerland. study such multi-trophic interactions [2,6]. This article is an open access article Herbicides are strong anthropogenic selection agents affecting weed evolution in distributed under the terms and con- agricultural systems, especially with the increase in herbicide use often associated with ditions of the Creative Commons At- the adoption of genetically modified herbicide-resistant (GMHR) crops [7]. In corn, cotton, tribution (CC BY) license (https:// and soybean, 89, 95, and 94% of the hectares in the US are planted with GMHR crops, creativecommons.org/licenses/by/ respectively [8], and herbicides are applied post crop emergence. The augmented herbicide 4.0/). Agronomy 2021, 11, 146. https://doi.org/10.3390/agronomy11010146 https://www.mdpi.com/journal/agronomy Agronomy 2021, 11, x 2 of 17 Agronomy 2021, 11, 146 2 of 16 and soybean, 89, 95, and 94% of the hectares in the US are planted with GMHR crops, respectively [8], and herbicides are applied post crop emergence. The augmented herbi- selectioncide selection pressure pressure in GMHR in GMHR systems systems is associated is associated with a greaterwith a frequencygreater frequency of establishment of estab- oflishment herbicide-resistant of herbicide (HR)-resistant weed (HR) biotypes. weed Currently,biotypes. Currently, there is a limited there is understanding a limited under- of thestanding dynamics of the of dynamics eco–evo (e.g., of eco weed–pathogen)–evo (e.g., weed interactions–pathogen) andinteractions the effect and of widespreadthe effect of agentswidespread of selection agents (e.g., of selection herbicide (e.g. use), inherbicide many agroecosystems use) in many where agroecosystems GMHR crops where are usedGMHR [2,9 crops,10]. In are some used instances, [2,9,10]. In plant some pathogens instances, (e.g., plant nematodes) pathogens may (e.g. disproportionately, nematodes) may impactdisproportionately select crop hosts impact and mayselect have crop evolved hosts and to have may a relativelyhave evolved minimal to have impact a relatively on other plantminimal hosts impact including on other weeds. plant In hosts the case including of nematodes, weeds. In this the may case be of especiallynematodes, true this since may theirbe especially range of movementtrue since istheir limited range with of movement passive dispersal, is limited thus with requiring passive a hostdispersal, to survive thus andrequiring reproduce a host [11 to,12 survive]. Additionally, and reproduce nematodes, [11,12] such. Additionally, as the soybean nematodes, cyst nematode such (SCN;as the Heteroderasoybean cyst glycines nematodeI.), are (SCN; known Heterodera to decrease glyc theines soybean I.), are canopyknown into susceptibledecrease the cultivars, soybean whichcanopy leads in susceptible to increased cultivars, weed densities which leads and weedto increased seed production weed densities at harvest and weed [13]. Thisseed increasedproduction potential at harvest for weed[13]. germinationThis increased and potential establishment for weed in the germination subsequent and season establish- feeds backment into in the the subsequent probability season of selecting feeds forback HR into weed the biotypesprobability with of herbicideselecting applicationsfor HR weed (Figurebiotypes1). with herbicide applications (Figure 1). FigureFigure 1. 1.Example Example ofof potentialpotential eco–evoeco–evo feedbacksfeedbacks inin thethe crop-weed–SCN-managementcrop-weed–SCN-management interaction in agroecosystems with reliance on herbicide for weed management. Created with BioRender® in agroecosystems with reliance on herbicide for weed management. Created with BioRender® (BioRender.com). (BioRender.com). 2.2. TheThe SCN–WeedSCN–Weed Host Host Relationship Relationship TheThe SCNSCN isis the main yield yield loss loss causing causing agent agent in in US US soybean, soybean, and and it is it widely is widely distrib- dis- tributeduted across across all all major major soybean soybean production production areas areas [14,15] [14,15].. In In a a survey survey conducted fromfrom2010 2010 toto 2014, 2014, losseslosses causedcaused by by SCNSCN inin thethe USUSwere were estimatedestimated to to be be doubledouble that that of of otherother diseases diseases nationwidenationwide [[16]16].. SCNSCN cancan causecause upup toto 60%60%of of yield yield losses losses when when susceptible susceptible cultivars cultivarsare are plantedplanted [17[17]],, and and up up to to 30% 30% in in loss loss without without showing showing aboveground aboveground symptoms symptoms [ 18[18]].. Hence Hence thethe emphasisemphasis for for the the needneed toto conductconduct properproper testing testing and and fieldfield scouting scouting [ 18[18––2020]] to to properly properly assessassess SCNSCN incidenceincidence inin productionproduction fields. fields. ToTo decrease decrease yield yield losses losses caused caused byby SCN,SCN, aa setset ofof integrated integrated pestpest managementmanagement (IPM)(IPM) practicespractices areare suggested,suggested, includingincluding usingusing resistantresistant soybeansoybean cultivars,cultivars, cropcrop rotationrotation withwith non-hosts,non-hosts, weedweed management,management, seed-applied seed-applied nematicides, nematicides, and and the the use use of of biological biological control control productsproducts [ 14[14,19,21,19,21––2626].]. In In fact, fact, a asingle single year yearin in aa weed-freeweed-free non-host non-host crop crop may may reduce reduce SCN SCN populationspopulations by by up up to to 55%55% [[2727]].. Currently,Currently, most most soybean soybean commercial commercial cultivars cultivars (>90%) (>90%) share share a common source of resistance (PI 88788), and the heavy reliance on this source of resistance led to the selection of SCN populations that
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