Free-Living Nematodes Together With Associated Microbes Play an Essential Role in Apple Replant Disease

Abstract

Apple replant disease (ARD) is a severe problem in apple production worldwide. It is caused by a complex of soil biota, leading to small discolorated roots, as well as increased biosynthesis of phytoalexins, total phenolic compounds and antioxidants. We sampled soil from randomized field plots with either apple trees affected by ARD, which were five times replanted every second year, or with healthy trees growing in plots, which had a grass cover during this period. We investigated the contribution of nematodes to ARD by dissecting the soil biota from plots infested with ARD and non-infested control plots into a nematode and a microbe fraction. Nematode communities significantly differed between ARD and control soil as revealed by high-throughput sequencing of 18S rRNA genes. Plant-parasitic nematodes were too low in abundance to explain root damage, and did not significantly differ between ARD and control soil. Their separate and synergistic effect on ARD symptoms of susceptible M26 apple rootstocks was analyzed 4 and 8 weeks after inoculation in three greenhouse experiments. Inoculants were either nematodes from ARD plots (NARD), NARD plus microbes from ARD plots (MARD), NARD plus microbes from control plots (MCon), nematodes from control plots NCon plus MARD, NCon plus MCon, MARD, or MCon, or non-inoculated control. In all three experiments, the combination NARD plus MARD had the strongest adverse effect on the plants, with respect to growth parameters of shoots and roots, total phenolic compounds and phytoalexins in roots, and antioxidants in leaves. NARD also induced ARD but less than NARD plus MARD. NARD plus MCon had delayed effects on the plants compared to NARD plus MARD, suggesting that detrimental nematode-microbe interactions built up with time. Effects of MARD or NCon plus MARD were minor or not distinguishable from those of MCon or non-inoculated control. Overall, the source of the inoculated nematodes -ARD or control soil- and the interaction between ARD nematodes and microbes were highly significant factors determining ARD. In conclusion, exploring the associations of nematodes and microbes in ARD soils will give the chance to unravel the etiology of ARD.

Reduced microbial potential for the degradation of phenolic compounds in the rhizosphere of apple plantlets grown in soils affected by replant disease

“…Yet, the presence of pathogenic nematodes cannot be excluded, as the methodology applied in our study was established to assess microbial communities and, hence, was inadequate for the detection of nematodes. However, plant-parasitic nematodes do not play a role on the occurrence of ARD in the soil of the site used in our experiment [23]. Overall, our data indicates that similar pathogen loads may lead to different plant growth patterns in virgin (CO) and ARD affected soils, with the last clearly causing disease symptoms.…”

Genes Involved in Stress Response and Especially in Phytoalexin Biosynthesis Are Upregulated in Four Malus Genotypes in Response to Apple Replant Disease

“…It is generally accepted that ARD is strongly associated with an unbalanced complex of soil biota, including bacteria, fungi, oomycetes, and nematodes (Rumberger et al, 2007;Kanfra et al, 2018). In the present study, the expression changes of 108 ARD CGs were evaluated in roots of three different Malus rootstocks and one wild apple genotype grown in ARD soils from two different sites in Germany.…”

Biofumigation for Fighting Replant Disease- A Review

“…With the arrival of new sequencing technologies, replanted soils have recently been subjected to concise microbial community analyses revealing pronounced changes in their structure as well as functions (e.g., [21][22][23][24]). Nematodes can contribute to apple replant disease either as phytopathogenic nematodes or free-living nematodes shaping microbial communities [25,26]. Studies on other soil organisms, especially of the mesofauna, are needed to better understand the complex changes in soil biota in replant situations.…”