Research Article: Potential role of weather, soil and plant microbial communities in rapid decline of apple trees

Date Published: March 6, 2019

Publisher: Public Library of Science

Author(s): Jugpreet Singh, Katchen Julliany Pereira Silva, Marc Fuchs, Awais Khan, Ricardo Aroca.


An unusual decline and collapse of young established trees known as “rapid apple decline” (RAD) has become a major concern for apple growers, particularly in the northeastern United States. This decline is characterized by stunted growth, pale yellow to reddish leaves, and tree collapse within weeks after onset of symptoms. We studied declining apple trees to identify potential involvement of abiotic and biotic stresses. We used 16S and ITS to profile bacterial and fungal communities in the soil, rhizosphere, roots, and shoots and tested for the presence of six viruses in scions and rootstocks of symptomatic and asymptomatic trees. The viruses detected were not associated with RAD symptoms. Bacterial and fungal populations were highly variable in plant tissue, soil and rhizosphere samples, with bacteroidetes, firmicutes, proteobacteria, acidobacteria, and actinobacteria the predominant bacterial classes in various samples. ‘Alphaproteobacteria-rickettsiales’, a bacterial class usually reduced in water-limiting soils, had significantly low abundance in root samples of symptomatic trees. Basidiomycota and Ascomycota fungal classes were the most common fungal classes observed, but neither showed differential enrichment between symptomatic and asymptomatic trees. Analyzing weather data showed an extremely cold winter followed by drought in 2015–2016, which likely weakened the trees to make them more susceptible to varied stresses. In addition, similar physical and nutritional soil composition from symptomatic and asymptomatic trees rules out the role of nutritional stress in RAD. Necrotic lesions and wood decay symptoms dispersing from bark or vascular cambium towards the heartwood were observed primarily below the graft union of declining apple trees, suggesting that the rootstock is the originating point of RAD. We speculate that differences in abiotic factors such as moisture levels in declining roots in combination with extreme weather profiles might cause RAD but cannot clearly rule out the involvement of other factors.

Partial Text

“Rapid apple decline” (RAD) describes a decline and collapse of young apple trees. This decline has become a major concern for growers in apple producing areas in the central, northeastern, and northwestern United States and in Ontario, Canada in recent years [1–4]. A similar situation was first described in north-central Washington State orchards in 1983 [5], and fifteen years later in southern British Columbia, Canada [6]. RAD is usually characterized by stunted tree growth, chlorotic canopy, and tree collapse within weeks after the onset of symptom development [2–4]. Symptoms generally first appear on one limb, with small, rolled leaves and reduced terminal growth, followed by the full tree canopy manifesting pale yellow to reddish leaves. Cankers and shedding are visible at the graft union, and wood necrosis progresses upstream to the trunk of the tree. The root system generally appears healthy, except that small feeder roots are absent [2, 5]. No common root rot pathogens or nutrient deficiency has been associated with RAD. After originating in one point of an orchard, the disorder seems to spread to adjacent trees. Symptomatic trees are usually removed from orchards due to poor productivity; however, if kept in the orchard, the symptoms may spread throughout the tree within a single year and ultimately lead to tree death.

Tree decline/death is often caused by diseases such as rootstock fire blight, phytophthora root and crown rots, or apple replant disease, or abiotic factors like soil wetness, extreme cold, spring and fall freezes, or drought, as well as injuries to trunk, graft union, crown and roots by rodents or insect borers. However, rapid or sudden decline of established apple trees (RAD), a recent concern to the apple industry, is diagnosed when symptoms do not match any of the above. We addressed this concern by conducting a comprehensive study to identify the role of soil nutrition, weather conditions, fungal and bacterial communities, as well as viruses in rapid decline of established ‘HoneyCrisp’ trees grafted onto the rootstock M.9 (clone NIC 29). Analysis of weather variables indicated abnormal trends at the experimental orchard site over the five-year growth period with December 2014, January, February and March 2015 being exceptionally cold. According to National Climate Report from the National Oceanic and Atmosphoric Administration (NOAA) National Centers for Environmental Information of the US, February 2015 was the third-coldest February on record in the region since 1934. In 2015, there were heavy rains between June-July followed by a severe drought in 2016 during the apple growing season. A severe temperature drop followed by a moderately warmer winter may have caused direct damage to apple trees or indirectly made them more susceptible to biotic and abiotic stresses [8, 9]. Both significant loss of trees and decrease in yield have previously occurred due to freezing temperatures in the United States and Canada [7, 42–45]. Cold injury symptoms become apparent in the spring following a hard winter with trees exhibiting stunted growth, wilting, and death. Rainfall data also indicated one drought instance in the area in 2016. Although no study has linked RAD with drought, general water stress can cause severe damage by reducing tree growth, root damage, and senescence [12–16, 46]. The occurrence of severe cold followed by drought, or either individually, might not directly cause RAD, but could have weakened the trees and led to the proliferation of insects and infection by opportunistic pathogens. Although the general soil fertility status was not optimal for commercial apple production [47], differences between soil nutrition profiles from symptomatic and asymptomatic apple trees were not significant, ruling out any potential role of nutritional stress in RAD in the experimental orchard. The concentrations of organic matter, total nitrogen, phosphorus, potassium, magnesium, and boron were all low in the experimental orchard area. Meanwhile, sulfur concentration was nearly two-fold over the recommended amount [47]. Nutritional differences might not directly contribute, but can exacerbate the impact of other stress factors such as weather extremes, insects, and pathogens, therefore increasing the chances of decline of apple trees. In some rootstock and scion combinations, a weak graft union can be impacted under extreme abiotic stresses, leading to a slow collapse of the tree. Also, rootstocks with shallow root-systems in high density plantings may have limited access to nutrients and water and thus be unable to support the heavy crop, foliage, and biomass under extreme weather, leading to decline and death of trees. The negative effect can be exacerbated in soils with poor water holding capacity.




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