Monitoring Effects of Rootstock Genotype and Soil Treatment Strategy on Postharvest Fruit Quality in ‘Gala’ Apple

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  • 1 Physiology and Pathology of Tree Fruits Research Unit, U.S. Department of Agriculture, Agricultural Research Service, 1104 North Western Avenue, Wenatchee, WA 98801

Production of high-quality tree fruit requires management of tree health and vigor during orchard establishment, especially with regard to soil-borne pathogens. Available strategies for the mitigation of soil-borne diseases include chemical fumigants, Brassicaceous seed meal (SM) soil treatments, and the use of disease-tolerant rootstock genotypes. It has been documented that superior disease suppression can be achieved using specific combinations of rootstock genotype and soil treatment that, in part, alter the soil microbiome. However, regardless of soil treatment strategy or rootstock genetics, sublethal levels of phytotoxic compounds are known to have negative effects on the reproductive output of plants. Yet the effects of SM amendments and the resultant restructuring of the soil microbiome on fruit quality are not well studied. Thus, our objective was to explore the effects of pathogen suppression strategies on at-harvest and postharvest fruit quality of ‘Gala’ apples (Malus domestica) by observing effects of both rootstock genetics [‘Malling 26’ (‘M.26’) vs. ‘Geneva 41’ (‘G.41’)] and soil treatment strategy (fumigation vs. SM). We observed that rootstock genotype generally appeared to have a stronger effect than soil treatment strategy on at-harvest fruit quality and postharvest outcomes. Further, although we did observe some fruit quality differences in each year of the study, there was no discernible pattern from year to year. We therefore conclude that, in our study, soil treatment does not have a consistent, significant influence on ‘Gala’ apple fruit quality, and importantly, efficacious ARD control using SM is without an apparent downside regarding fruit quality.

Abstract

Production of high-quality tree fruit requires management of tree health and vigor during orchard establishment, especially with regard to soil-borne pathogens. Available strategies for the mitigation of soil-borne diseases include chemical fumigants, Brassicaceous seed meal (SM) soil treatments, and the use of disease-tolerant rootstock genotypes. It has been documented that superior disease suppression can be achieved using specific combinations of rootstock genotype and soil treatment that, in part, alter the soil microbiome. However, regardless of soil treatment strategy or rootstock genetics, sublethal levels of phytotoxic compounds are known to have negative effects on the reproductive output of plants. Yet the effects of SM amendments and the resultant restructuring of the soil microbiome on fruit quality are not well studied. Thus, our objective was to explore the effects of pathogen suppression strategies on at-harvest and postharvest fruit quality of ‘Gala’ apples (Malus domestica) by observing effects of both rootstock genetics [‘Malling 26’ (‘M.26’) vs. ‘Geneva 41’ (‘G.41’)] and soil treatment strategy (fumigation vs. SM). We observed that rootstock genotype generally appeared to have a stronger effect than soil treatment strategy on at-harvest fruit quality and postharvest outcomes. Further, although we did observe some fruit quality differences in each year of the study, there was no discernible pattern from year to year. We therefore conclude that, in our study, soil treatment does not have a consistent, significant influence on ‘Gala’ apple fruit quality, and importantly, efficacious ARD control using SM is without an apparent downside regarding fruit quality.

The tree fruit production environment influences apple fruit quality. Interactions between environmental conditions and scion–rootstock combinations can lead to differences in fruit quality within the same cultivar and across years (Corelli-Grappadelli and Lakso, 2004; Musacchi and Serra, 2018). To optimize fruit production, specific combinations of scion, rootstock, and orchard management strategies based on the local environment should be selected during orchard establishment (D’Abrosca et al., 2017; Lordan et al., 2019; Reig et al., 2019). Over the past several decades orchards have been turned over and replanted with new, higher density planting systems. A persistent challenge in managing tree health and vigor at the onset of orchard establishment has been how to mitigate complex, soil-borne diseases, such as apple replant disease (ARD) (Savory, 1966).

Historically, chemical fumigants have been used as an effective method to control ARD (Covey et al., 1979; Mai and Abawi, 1981; Pitcher et al., 1966). However, agrochemical use has been under increasing scrutiny over the past several decades (Holmes et al., 2020; López-Aranda et al., 2016; Reeve et al., 2016), resulting in widespread governmental regulations limiting or prohibiting the use of certain fumigants. As consumer attitude toward the use of agrochemicals has evolved, increasing emphasis has been placed on identifying effective alternative tools for controlling pathogenic microbe communities within agricultural soil (Caputo et al., 2015; Forge et al., 2016; Kandula et al., 2010; Ruzo, 2006; Watson et al., 2019).

During the early stages of orchard establishment, one of the tools commonly used to mitigate the negative effects of soil-borne pathogens is through the selection of an appropriate rootstock genotype. Over the past several decades, rootstocks have been bred to influence critical aspects of tree health and fruit production, such as vigor, crop yield, fruit size, drought tolerance, nutrient uptake, and disease tolerance (Atkinson, 2001; Cummins and Aldwinckle, 1983; Nimbolkar et al., 2016; Valverdi and Kalcsits, 2021; Warschefsky et al., 2016). Rootstocks have been shown to alter the scion’s response to biotic and abiotic stress (Jensen et al., 2010). Rootstock genotype also influences microbiome community composition of the rhizosphere (Aira et al., 2010; Bodenhausen et al., 2014; Bouffaud et al., 2012; Peiffer et al., 2013) as well as the endophytic microbiome (Van Horn et al., 2021). Furthermore, certain soil microbiome community members may impart functional benefits to the plant such as mediating biotic and abiotic stressors (Castillo-Lopez et al., 2014; Rodriguez et al., 2010).

The application of Brassicaceous SM to soil generates various glucosinolate hydrolysis products. These hydrolysis products are generally toxic and have wide-ranging effects on microorganisms and plants (Brown and Morra, 1997). Glucosinolate hydrolysis products have also been observed to alter nutrient availability and content (Cohen et al., 2005; Omirou et al., 2011; Wang et al., 2014). The combination of toxins and altered nutrient profiles in the soil results in a restructuring of the microbial community, ideally by suppressing pathogens and promoting microorganisms with beneficial functions such as nitrogen-cycling and sulfur-oxidation (Mazzola et al., 2015; Raaijmakers and Mazzola, 2016). However, the overall effect of these soil alterations on the microbial community is highly dependent on the incumbent microbial community’s composition and the tolerance of incumbent community members to the various hydrolysis products (Galletti et al., 2008). Overall, the efficacy of SM treatments on the successful suppression of disease depends on a variety of factors such as the composition of the soil microbiome community at the time of application, the correct identification of the target pathogen(s), pairing target pathogens with the proper source of SM (Cohen and Mazzola, 2006; Mazzola et al., 2007, 2001; Weerakoon et al., 2012), and the selection of an apple rootstock with the desired genotype-specific interaction with the soil microbiome (Mazzola et al., 2015; St. Laurent et al., 2010).

Chemical fumigants and SMs containing glucosinolate are also used for weed control in orchards due to their phytotoxicity. If tree saplings are planted too soon after application, the saplings could be exposed to phytotoxins, which can result in tree death (Handiseni et al., 2013). In field trial comparisons between Malling and Geneva® series rootstocks, it has also been observed that even if the recommended period elapses between SM treatments and orchard establishment, trees grown on some Malling series rootstocks may still show signs of stress and can even die (Mazzola et al., 2015; Wang and Mazzola, 2019a). It is therefore possible that orchard trees are exposed to sublethal doses of phytotoxins, whereafter they recover from such sublethal stress events (Marrs et al., 1991; Riemens et al., 2008, 2009). Despite the probability of recovery of plant biomass over time, the energetic expenses required for recovery can have a negative effect on a plant’s future reproductive output (Carpenter and Boutin, 2010), such as a reduction in flower and seed production (Kjær et al., 2006; Riemens et al., 2009), and decreases in crop yield which have been observed in potato (Pfleeger et al., 2008), sorghum (Al-Khatib et al., 2003), and cherry (Bhatti et al., 1995).

Recent studies in Washington State have shown that the use of SM in combination with certain rootstocks (e.g., Geneva® series rootstocks) can significantly alter soil microbiome and the rhizosphere community to mitigate apple replant disease (Mazzola et al., 2009, 2015; Wang and Mazzola, 2019a, 2019b). A recent field trial in north-central Washington State focused on identifying the effects of the interaction among four soil treatments [2.2, 4.4, and 6.6 t per hectare (t·ha−1) SM, and a traditional fumigant] and a no treatment control with two rootstock genotypes, ‘M.26’ [ARD susceptible (Costante et al., 1987 Reim et al., 2019)] and ‘Geneva 41’ [‘G.41’, ARD tolerant (Isutsa and Merwin, 2000; Reim et al., 2019; Robinson et al., 2011)] on the soil microbiome community as it related to ARD (Wang and Mazzola, 2019a). In addition to effects on the soil microbiome, differences in tree growth, tree mortality, and crop yields were observed among soil treatments and rootstock genotype comparisons (Wang and Mazzola, 2019a). Briefly, this study observed higher tree mortality, less growth, and lower yields for trees grown on the ‘M.26’ rootstock and treated at the highest SM amendment 6.6 t·ha−1 compared with those grown on the ‘G.41’ rootstock; the authors hypothesized that this was likely a result of mortality and growth suppression due to phytotoxicity in the ‘M.26’ rootstock during the first growing season (Wang and Mazzola, 2019a). At lower SM amendment rates and in the fumigated treatment, trees grown on the ‘M.26’ rootstock had a larger trunk diameter than ‘G.41’, while those grown on the ‘G.41’ rootstock had higher crop yields than ‘M.26’.

Preharvest conditions affect postharvest outcomes (Watkins and Mattheis, 2019). Thus, a greater understanding of interactions among scion genotypes, rootstock genotypes, soil microbiomes, local environments, and orchard management practices is needed to properly integrate preharvest microbiome-based management practices with optimal postharvest fruit quality outcomes (Busby et al., 2017; Jacoby et al., 2021). Recent attention to the effects of preharvest conditions on postharvest outcomes has been given to apple production as it relates to rootstock genotype and growing environment (Donahue et al., 2021; Reig et al., 2019; Yuri et al., 2019), but few studies have explored the effects of soil treatments on at-harvest or postharvest fruit quality. The recent field trial set up by Wang and Mazzola (2019a) provided a unique opportunity to observe longer term effects of soil treatments, specifically Brassicaceous SM, and rootstock genetics on ‘Gala’ tree fruit quality while controlling for environmental variables. Our objective of this study was to observe the effects of preplant soil treatment and rootstock genotype on ‘Gala’ fruit quality both at-harvest and into the postharvest period.

Methods

Orchard site and block description.

Fruit was harvested from ‘Gala’ trees grown at the Washington State University/U.S. Department of Agriculture–Agricultural Research Service (USDA-ARS) Columbia View Research and Demonstration Orchard near East Wenatchee, WA (lat. 47°37′33″ N, long. 120°13′31″ W). The orchard used for this study was the site for a field trial which examined the efficacy of disease suppression, tree survival, and the medium-term effect on fruit yield of various soil treatments on ‘Gala’ apple. This orchard was chosen as the site for a follow-up study based on the results of Wang and Mazzola (2019a, 2019b), where field trials showed important differences in tree growth, tree mortality, and crop load among rootstock and soil amendment comparisons (Wang and Mazzola, 2019a).

Fumigation plots were treated with 1,3-dichloropropene-chloropicrion (Telone C-35; Corteva AgriScience, Wilmington, DE) in Oct. 2015. Seed meal treatments [1:1 mixture Brassica juncea/Sinapis alba (Farm Fuel Inc., Santa Cruz, CA)] of 2.2, 4.4, and 6.6 t·ha−1 were applied the following spring in Apr. 2016. On 1 June 2016, 15-mm caliper ‘Gala’ scions grafted onto either ‘M.26’ or ‘G.41’ rootstocks (Van Well Nursery, East Wenatchee, WA) were planted. For the first 2 years after the orchard was planted, trees were minimally managed using standard pesticide applications and trimmed to prevent limb breakage (M. Mazzola, personal communication). Then, during the 2019 and 2020 growing seasons, trees were managed according to standard commercial practices to optimize fruit quality, including crop thinning to minimize the impact of crop load variation on fruit quality metrics. See Supplemental Fig. S1 for soil treatment application and rootstock planting layout within the orchard block. For full details on soil treatment and rootstock randomization and experimental design, consult Wang and Mazzola (2019a).

Fruit harvest and storage.

Fruit from each rootstock and soil treatment combination were harvested 2 years in a row, on 3 Sept. 2019 and 27 Aug. 2020. Approximately 10 to 15 pieces of fruit were harvested across all replicate trees in each treatment in both harvest years. Fruit from each rootstock × soil treatment combination were harvested into separate boxes in the field and then brought to the USDA-ARS Tree Fruit Research Laboratory in Wenatchee, WA. Upon arrival, apples within each rootstock × soil treatment combination were pooled and randomly sorted by hand onto pressed fiber fruit trays, with 18 fruit to a tray. Then, trays were placed in cardboard boxes (three trays to a box) and stored in air at 1 °C for 10 weeks (2019 harvest) or 14 weeks (2020 harvest).

Fruit quality assessment.

For each rootstock × soil treatment, fruit quality was assessed at harvest (n = 18) and at three postharvest timepoints: in 2019 at 4, 8, and 10 weeks postharvest and in 2020 at 6, 10, and 14 weeks postharvest. At each postharvest time point, 18 fruit were removed for each rootstock × soil treatment and placed in a dark room at 20 °C for 7 d to simulate time in a supply chain. After 7 d, ‘ripened’ fruit were subject to a full quality assessment (raw quality data can be found in Supplemental File S1 datasets).

Fruit quality and maturity were assessed by analyzing both external and internal parameters, including weight, color [L*a*b derived hue and chroma (CR-300 Colorimeter; Minolta, Tokyo, Japan)], red color percent coverage (harvest only), background color [Unifruco Research Services (PTY) Ltd., South Africa, 1991; Color Chart for Apples and Pears), internal ethylene concentration (8890 GC System; Agilent, Santa Clara, CA), firmness and texture (MDT-2, MOHR, Richland, WA), titratable acidity (Titrator Excellence T5 with InMotion Pro AutoSampler; Mettler Toledo, Columbus, OH), and soluble solids content [expressed as Brix° (Brix N1 Refractometer; Atago, Tokyo, Japan)]. A summary of fruit quality assessments and brief descriptions of measurements are reported in Table 1.

Table 1.

A list of fruit quality parameters, used throughout the paper and supplementary files, as well as a brief description of the parameter and the instrument used to collect the data (where applicable). For flesh firmness metrics assessed using the MDT-2 Mohr Penetrometer: Region 1 (R1) is specified by the fixed depth from the outermost edge of the fruit to a depth of 0.32 inch (Mohr and Mohr, 2007). Region 2 (R2) is an arbitrary depth that extends from the end of R1 to a depth proportional to 30% of the diameter of the fruit. For additional details regarding force measurements, consult exhaustive summaries by Evans et al. (2010), Mohr (2002, 2012), Mohr and Mohr (2007), and Teh et al. (2020).

Table 1.

Statistical analysis.

All data were analyzed using R v4.0.3 (R Core Team, 2020). Before analyses of variance, Levene’s test was used to test for homogeneity of variance with the R package ‘car’ v3.0-10 (Fox and Weisberg, 2019). Results from Levene’s test for homogeneity of variance can be found in Supplemental File S2. To compare effects of soil treatments within a rootstock, a one-way analysis of variance with the Tukey honest significant differences correction (base R function tukeyHSD(); Tukey, 1949) for multiple pairwise comparisons was performed. For those comparisons that failed Levene’s test for homogeneity of variance, Welch’s one-way test with the Games-Howell post hoc test for multiple comparisons (Lee and Lee, 2018; Toothaker, 1993) was performed using the R package ‘rstatix’ v0.6.0 (Kassambara, 2020). To compare the rootstock effect within each soil treatment, Welch’s t test was performed using the t.test() function in base R, with the var.equal parameter set to FALSE (R Core Team, 2020).

Results

Overall, neither soil treatment nor rootstock genotype had a consistently strong effect on ‘Gala’ fruit quality across the 2019 and 2020 harvest seasons. There were more statistically significant differences in fruit quality parameters between treatments in 2019 compared with the 2020 harvest season (Figs. 13). In both study years, fruit grown in untreated (control) soil had the most similar at-harvest and postharvest quality (Figs. 46) when comparing between rootstock genotypes. Fruit grown in amended soil, regardless of amendment strategy used, had more disparate quality between rootstock genotypes both at harvest and into the postharvest period. However, by which quality metrics they differed was inconsistent from year to year.

Fig. 1.
Fig. 1.

Apple rootstock genotype has a greater influence on at-harvest apple fruit quality than soil treatment. Although the rootstock genotype has a greater effect, there is no consistent pattern across years, with some fruit quality parameters showing opposite patterns in the 2 study years. At-harvest ‘Gala’ apple fruit quality from the 2019 and 2020 harvest seasons. Values are means (n = 18) ± se for each rootstock genotype (RG) by soil treatment (ST). Significant differences in pairwise t test results between RGs ‘Malling 26’ (‘M.26’) and ‘Geneva 41’ (‘G.41’) within each ST are indicated via shading according to their P value threshold. zCtl = control treatment; Fum = fumigation treatment; SM2 = seed meal (SM) application rate of 2.2 t·ha−1; SM4 = SM application rate of 4.4 t·ha−1. SM application consisted of a 1:1 mixture Brassica juncea/Sinapis alba. The fumigation treatment was an application of 1,3-dichloropropene-chloropicrion (Telone C-35). yWeight (g); diameter (cm); starch index (1–6); Brix° = suspended solids; TA = titratable acidity; IEC = internal ethylene concentration (μL·L−1); Red % = red overcolor percent coverage; Red h° = Red color hue angle; Red Chroma = red color chroma; Ground h° = background color hue angle; Ground Chroma = background color chroma; OMH = overall maximum hardness (N); M1 = maximum hardness region 1 (N); Qf = overall quality factor.

Citation: HortScience 57, 7; 10.21273/HORTSCI16407-21

Fig. 2.
Fig. 2.

In 2019, soil treatment did not have a consistent strong effect on at-harvest fruit quality. To emphasize the tests for soil treatment effects, we reorganized the data presentation for at-harvest fruit quality of ‘Gala’ apple fruit in 2019 alone. For instance, if a treatment had a strong and consistent effect, significant differences would be concentrated in columns for that treatment; we did not observe this pattern. Values are means (n = 18) ± se for each rootstock genotype (RG) by soil treatment (ST). Significant differences from analysis of variance with the Tukey honest significant differences correction for multiple pairwise comparisons were performed, with results indicated via shading according to their P value threshold. zST = soil treatment; Ctl = control treatment; Fum = fumigation treatment; SM2 = seed meal (SM) application rate of 2.2 t·ha−1; SM4 = SM application rate of 4.4 t·ha−1. SM application consisted of a 1:1 mixture Brassica juncea/Sinapis alba. The fumigation treatment was an application of 1,3-dichloropropene-chloropicrion (Telone C-35). yRG = rootstock genotype; ‘Malling 26’ (‘M.26’); ‘Geneva 41’ (‘G.41’). xWeight (g); diameter (cm); starch index (1–6); Brix° = suspended solids; TA = titratable acidity; IEC = internal ethylene concentration (μL·L−1); Red % = red overcolor percent coverage; Red h° = red color hue angle; Red Chroma = red color chroma; Ground h° = background color hue angle; Ground Chroma = background color chroma; OMH = overall maximum hardness (N); M1 = maximum hardness region 1 (N); Qf = overall quality factor.

Citation: HortScience 57, 7; 10.21273/HORTSCI16407-21

Fig. 3.
Fig. 3.

In 2020, soil treatment did not have a consistent strong effect on at-harvest fruit quality. As in Fig. 2, to emphasize the tests for soil treatment effects, we reorganized the data presentation for at-harvest fruit quality of ‘Gala’ apple fruit, but for the second study year, 2020. For instance, if a treatment had a strong and consistent effect, significant differences would be concentrated in columns for that treatment; we did not observe this pattern. At harvest ‘Gala’ apple fruit quality from the 2020 harvest season. Values are means (n = 18) ± se for each rootstock genotype (RG) by soil treatment (ST). Significant differences from analysis of variance with the Tukey honest significant differences correction for multiple pairwise comparisons were performed, with results indicated via shading according to their P value threshold. zST = soil treatment; Ctl = control treatment; Fum = fumigation treatment; SM2 = seed meal (SM) application rate of 2.2 t·ha−1; SM4 = SM application rate of 4.4 t·ha−1. SM application consisted of a 1:1 mixture Brassica juncea/Sinapis alba. The fumigation treatment was an application of 1,3-dichloropropene-chloropicrion (Telone C-35). yRG = rootstock genotype; ‘Malling 26’ (‘M.26’); ‘Geneva 41’ (‘G.41’). xWeight (g); diameter (cm); starch index (1–6); Brix° = suspended solids; TA = titratable acidity; IEC = internal ethylene concentration (μL·L−1); Red % = red overcolor percent coverage; Red h° = red color hue angle; Red Chroma = red color chroma; Ground h° = background color hue angle; Ground Chroma = background color chroma; OMH = overall maximum hardness (N); M1 = maximum hardness region 1 (N); Qf = overall quality factor.

Citation: HortScience 57, 7; 10.21273/HORTSCI16407-21

Fig. 4.
Fig. 4.

Apple rootstock genotype has a greater influence on postharvest apple fruit quality than soil treatment. Similar to at-harvest data, after 10 weeks of cold storage in air the rootstock genotype still has a greater effect on fruit quality. Fruit quality changed largely as expected during the postharvest period, with at-harvest patterns persisting. Postharvest ‘Gala’ apple fruit quality after 10 weeks of cold storage from both the 2019 and 2020 harvest seasons is shown. Values are means (n = 18) ± se for each rootstock genotype (RG) by soil treatment (ST). Significant differences in pairwise t test results between RGs ‘Malling 26’ (‘M.26’) and ‘Geneva 41’ (‘G.41’) within each ST are indicated via shading according to their P value threshold. zST = soil treatment; Ctl = control treatment; Fum = fumigation treatment; SM2 = seed meal (SM) application rate of 2.2 t·ha−1; SM4 = SM application rate of 4.4 t·ha−1. SM application consisted of a 1:1 mixture Brassica juncea/Sinapis alba. The fumigation treatment was an application of 1,3-dichloropropene-chloropicrion (Telone C-35). yRG = rootstock genotype; ‘Malling 26’ (‘M.26’); ‘Geneva 41’ (‘G.41’). xWeight (g); diameter (cm); starch index (1–6); Brix° = suspended solids; TA = titratable acidity; IEC = internal ethylene concentration (μL·L−1); Red % = red overcolor percent coverage; Red h° = red color hue angle; Red Chroma = red color chroma; Ground h° = background color hue angle; Ground Chroma = background color chroma; OMH = overall maximum hardness (N); M1 = maximum hardness region 1 (N); Qf = overall quality factor.

Citation: HortScience 57, 7; 10.21273/HORTSCI16407-21

Fig. 5.
Fig. 5.

In 2019, soil treatment did not have a consistent strong effect on postharvest fruit quality. To emphasize the tests for soil treatment effects, we reorganized the data presentation for postharvest fruit quality of ‘Gala’ apple fruit in 2019 alone. For instance, if a treatment had a strong and consistent effect after 10 weeks of cold storage in air, significant differences would be concentrated in columns for that treatment; we did not observe this pattern. Values are means (n = 18) ± se for each rootstock genotype (RG) by soil treatment (ST). Significant differences from analysis of variance with the Tukey honest significant differences correction for multiple pairwise comparisons were performed, with results indicated via shading according to their P value threshold. zST = soil treatment; Ctl = control treatment; Fum = fumigation treatment; SM2 = seed meal (SM) application rate of 2.2 t·ha−1; SM4 = SM application rate of 4.4 t·ha−1. SM application consisted of a 1:1 mixture Brassica juncea/Sinapis alba. The fumigation treatment was an application of 1,3-dichloropropene-chloropicrion (Telone C-35). yRG = rootstock genotype; ‘Malling 26’ (‘M.26’); ‘Geneva 41’ (‘G.41’). xWeight (g); diameter (cm); starch index (1–6); Brix° = suspended solids; TA = titratable acidity; IEC = internal ethylene concentration (μL·L−1); Red % = red overcolor percent coverage; Red h° = red color hue angle; Red Chroma = red color chroma; Ground h° = background color hue angle; Ground Chroma = background color chroma; OMH = overall maximum hardness (N); M1 = maximum hardness region 1 (N); Qf = overall quality factor.

Citation: HortScience 57, 7; 10.21273/HORTSCI16407-21

Fig. 6.
Fig. 6.

In 2020, soil treatment did not have a consistent strong effect on postharvest fruit quality. To emphasize the tests for soil treatment effects, we reorganized the data presentation for postharvest fruit quality of ‘Gala’ apple fruit in 2020 alone. For instance, if a treatment had a strong and consistent effect after 10 weeks of cold storage in air, significant differences would be concentrated in columns for that treatment; we did not observe this pattern. Values are means (n = 18) ± se for each rootstock genotype (RG) by soil treatment (ST). Significant differences from analysis of variance with the Tukey honest significant differences correction for multiple pairwise comparisons were performed, with results indicated via shading according to their P value threshold. zST = soil treatment; Ctl = control treatment; Fum = fumigation treatment; SM2 = seed meal (SM) application rate of 2.2 t·ha−1; SM4 = SM application rate of 4.4 t·ha−1. SM application consisted of a 1:1 mixture Brassica juncea/Sinapis alba. The fumigation treatment was an application of 1,3-dichloropropene-chloropicrion (Telone C-35). yRG = rootstock genotype; RGs ‘Malling 26’ (‘M.26’) and ‘Geneva 41’ (‘G.41’). xWeight (g); diameter (cm); starch index (1–6); Brix° = suspended solids; TA = titratable acidity; IEC = internal ethylene concentration (μL·L−1); Red % = red overcolor percent coverage; Red h° = red color hue angle; Red Chroma = red color chroma; Ground h° = background color hue angle; Ground Chroma = background color chroma; OMH = overall maximum hardness (N); M1 = maximum hardness region 1 (N); Qf = overall quality factor.

Citation: HortScience 57, 7; 10.21273/HORTSCI16407-21

At the time of the 2019 harvest, a high prevalence of stem bowl splitting and bird pecks were noted. Fruit with stem bowl splits and bird pecks were not harvested. Due to the high prevalence of fruit damage, a limited amount of fruit in the ‘G.41’ control treatment was available for postharvest quality assessment. In addition, due to previous tree death as a result of phytotoxicity or ARD (or both), a limited amount of fruit was available for postharvest quality assessment in the ‘M.26’ 6.6 t·ha−1 treatment; fruit for these two rootstock × soil treatment were not assessed at the 8-week time point for the 2019 harvest season.

Fruit flesh firmness.

The most consistent difference observed across both harvest seasons was in flesh firmness (M1); fruit grown on ‘M.26’ rootstock was significantly firmer at harvest compared with those grown on ‘G.41’, irrespective of soil treatment (Fig. 1). The at-harvest differences in flesh firmness were not maintained during storage, and all fruit regardless of soil treatment or rootstock genotype were of similar flesh firmness at the conclusion of the postharvest period for both years of study (Fig. 4). We note that where significant differences in flesh firmness did occur, these differences did not always correspond with a significant disparity in fruit size or vice versa (Figs. 16).

Fruit size.

Rootstock genotype had either weakly or nonsignificant effects on at-harvest fruit size, with fruit grown on ‘G.41’ rootstock being generally larger than those grown on the ‘M.26’ rootstock, although significant differences were not consistent across harvest seasons (Fig. 1). Fruit grown in fumigated soil and the lowest seed meal application rate tended to be larger than fruit grown in control soil; however, this effect was also not consistent between harvest years (Figs. 2 and 3). Rootstock and soil treatment effects on fruit size were maintained through the postharvest period. Fruit grown in the highest SM treatment (6.6 t·ha−1) on the ‘M.26’ rootstock also tended to be smaller than those grown in soil treated at the lower rates of SM application and fumigated soils (Supplemental File S2).

Fruit peel color.

Differences in at-harvest peel color were observed between rootstock genotypes at harvest, ranging from nonsignificant to weakly significant. Fruit grown on the ‘G.41’ rootstock had less red coloration (higher Red h° and Red Chroma values; Fig. 1) and a yellower background color (high Ground h° and Ground Chroma values; Fig. 1) compared with fruit grown on the ‘M.26’ rootstock, although these observations were not consistent between harvest seasons (Fig. 1). Neither rootstock nor soil treatment demonstrated a strong effect on postharvest peel color development (Figs. 46). All fruit regardless of rootstock genotype and soil treatment had similar peel color profiles after postharvest storage during both study years (Figs. 46).

Discussion

Apart from there being fewer overall differences in fruit quality (both at harvest and in the postharvest period) in 2020 compared with 2019, there were no strong trends between each harvest season. High variability in fruit quality between years and lack of strong patterns is not without precedent in studies focusing on the impact of rootstock and environmental factors on fruit quality (Donahue et al., 2021; Reig et al., 2019; Yuri et al., 2019). Differences observed in fruit quality across years in this experiment could be due to subtle differences in at-harvest maturity. Fruit during the 2019 harvest season were noted to have a high number of stem bowl splits, indicative of fruit with more advanced maturity. The most consistent difference observed was in flesh firmness, with fruit grown on ‘M.26’ rootstock being significantly firmer at harvest than ‘G.41’. However, these differences may not translate to noticeable disparities by consumers, as consumers do not typically detect differences in firmness that are less than 6 Newtons (Harker et al., 2002).

Rootstock genotype ‘M.26’ was selected for the original experiment because of its susceptibility to apple replant disease (Wang and Mazzola, 2019a). Compared with the ‘G.41’ rootstock genotype, ‘M.26’ has comparatively more inconsistent vigor and canopy size and is prone to biennial bearing (Warner, 2011), which may have contributed to the inconsistencies in fruit quality patterns observed between the two harvest seasons in this study. Additionally, tree architecture and vigor influence the light environment experienced by the fruit, as well as affect crop load (Hewett, 2006). Both light environment and crop load affect many different aspects of fruit maturity and quality, especially for the development of red coloration, one of the most important traits tied to consumer preference and market value (Marsh et al., 1996; Musacchi and Serra, 2018). Dwarfing rootstocks such as ‘M.26’ have a reduced canopy size that creates a more uniform distribution of sunlight across the canopy. This more uniform distribution of sunlight generally results in a more desirable red peel color (Reay and Lancaster, 2001; Telias et al., 2011), which is consistent with our observations regarding the redder color of fruit from the ‘M.26’ rootstock genotype compared with ‘G.41’.

Although rootstock genotype appears to have a greater effect on fruit quality compared with soil treatments, it is possible that the effects of soil treatment on fruit quality decrease overtime. Trees in this block were established in 2016, and fruit quality assessment was done in years 3 and 4 after establishment. Increasing the length of time between sublethal stress events during orchard establishment and fruit harvest could be giving trees a longer time to recover from stress events. Indeed, for trees grown in the highest rate of SM application (6.6 t·ha−1), harvested fruit tended to be smaller than those from trees grown in soil amended at the lower rates of SM application and fumigated soils. These observations suggest that severe stress experienced by trees during orchard establishment due to high rates of SM application (Wang and Mazzola, 2019a) could negatively affect fruit size several years after orchard establishment on surviving trees.

It is also possible that site-specific characteristics as they relate to pathogen load or abiotic soil features may contribute to the magnitude rootstock genotype or soil treatment strategy effects on fruit quality. The plot this study was conducted in has historically been observed to have a low pathogen load (Mazzola and Brown, 2010; Mazzola and Mullinix, 2005; Wang and Mazzola, 2019a), which could partially explain why we observed sporadic differences in fruit quality in both years, and no clear patterns that could be attributable to the soil treatment were observed. In different orchards with higher disease pressure, it is possible that more clear patterns could emerge. Further, an expanded experiment incorporating additional years, sites, rootstocks, and other parameters would allow us to explore interactions among factors that our experimental design did not permit.

Overall, results from this study indicate that the disease suppression strategy does not have a clear effect on at-harvest or postharvest fruit quality. Potential long-term, sublethal phytotoxic effects on fruit quality were not seen in low and moderate (2.2 to 4.4 t·ha−1) rates of SM application. Importantly, the positive effects on fruit yield and tree health that accompany disease suppression by SM application, which persists longer than chemical fumigation, are accompanied by no clear patterns of at-harvest or postharvest reduction of fruit quality.

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Supplemental Fig. S1.
Supplemental Fig. S1.

Map of tree establishment on 1 June 2016. This block is located within the Washington State University/United States Department of Agriculture-Agricultural Research Service Columbia View Research and Demonstration Orchard near East Wenatchee, WA (N 47° 37′ 33″, W 120° 13′ 31″). The map used here was adapted from Wang and Mazzola (2019). Background color indicates the type of soil amendment used. Each row has 4 soil amendment sections. Each soil amendment section was approximately 10.5 m in length and divided into two sections, one section was planted with five ‘Gala’ scion grafted onto rootstock genotype ‘Malling 26’ (‘M.26’), and the other section was planted with five ‘Gala’ scion grafted onto rootstock genotype ‘Geneva 41’ (‘G.41’). Each section contained 10 total trees. Within each row, a 1.5 m space separated each soil amendment section. Rows were spaced approximately 4.5 m apart. During the first two years of growth, trees were minimally managed using standard pesticide applications and trimmed to prevent limb breakage (M. Mazzola, personal communication). After the 2018 growing season, trees were managed according to standard commercial practices to optimize fruit quality.

Citation: HortScience 57, 7; 10.21273/HORTSCI16407-21

Contributor Notes

We thank Allison Kane for expert assistance in sample processing and Bruno Torres and Sophia Reed for sample collection and processing. This work was funded by the U.S. Department of Agriculture’s (USDA) Agricultural Research Service. Mention of a trademark, proprietary product, or vendor in this publication is solely for the purpose of providing scientific information and does not constitute a guarantee or warranty of the product, imply recommendation or endorsement, nor imply its approval to the exclusion of other products or vendors that also may be suitable by the U.S. Department of Agriculture. The findings and conclusions in this publication are those of the authors and should not be construed to represent any official USDA or U.S. Government determination or policy. The USDA is an equal opportunity provider and employer.

L.H. is the corresponding author. E-mail: loren.honaas@usda.gov.

  • View in gallery

    Apple rootstock genotype has a greater influence on at-harvest apple fruit quality than soil treatment. Although the rootstock genotype has a greater effect, there is no consistent pattern across years, with some fruit quality parameters showing opposite patterns in the 2 study years. At-harvest ‘Gala’ apple fruit quality from the 2019 and 2020 harvest seasons. Values are means (n = 18) ± se for each rootstock genotype (RG) by soil treatment (ST). Significant differences in pairwise t test results between RGs ‘Malling 26’ (‘M.26’) and ‘Geneva 41’ (‘G.41’) within each ST are indicated via shading according to their P value threshold. zCtl = control treatment; Fum = fumigation treatment; SM2 = seed meal (SM) application rate of 2.2 t·ha−1; SM4 = SM application rate of 4.4 t·ha−1. SM application consisted of a 1:1 mixture Brassica juncea/Sinapis alba. The fumigation treatment was an application of 1,3-dichloropropene-chloropicrion (Telone C-35). yWeight (g); diameter (cm); starch index (1–6); Brix° = suspended solids; TA = titratable acidity; IEC = internal ethylene concentration (μL·L−1); Red % = red overcolor percent coverage; Red h° = Red color hue angle; Red Chroma = red color chroma; Ground h° = background color hue angle; Ground Chroma = background color chroma; OMH = overall maximum hardness (N); M1 = maximum hardness region 1 (N); Qf = overall quality factor.

  • View in gallery

    In 2019, soil treatment did not have a consistent strong effect on at-harvest fruit quality. To emphasize the tests for soil treatment effects, we reorganized the data presentation for at-harvest fruit quality of ‘Gala’ apple fruit in 2019 alone. For instance, if a treatment had a strong and consistent effect, significant differences would be concentrated in columns for that treatment; we did not observe this pattern. Values are means (n = 18) ± se for each rootstock genotype (RG) by soil treatment (ST). Significant differences from analysis of variance with the Tukey honest significant differences correction for multiple pairwise comparisons were performed, with results indicated via shading according to their P value threshold. zST = soil treatment; Ctl = control treatment; Fum = fumigation treatment; SM2 = seed meal (SM) application rate of 2.2 t·ha−1; SM4 = SM application rate of 4.4 t·ha−1. SM application consisted of a 1:1 mixture Brassica juncea/Sinapis alba. The fumigation treatment was an application of 1,3-dichloropropene-chloropicrion (Telone C-35). yRG = rootstock genotype; ‘Malling 26’ (‘M.26’); ‘Geneva 41’ (‘G.41’). xWeight (g); diameter (cm); starch index (1–6); Brix° = suspended solids; TA = titratable acidity; IEC = internal ethylene concentration (μL·L−1); Red % = red overcolor percent coverage; Red h° = red color hue angle; Red Chroma = red color chroma; Ground h° = background color hue angle; Ground Chroma = background color chroma; OMH = overall maximum hardness (N); M1 = maximum hardness region 1 (N); Qf = overall quality factor.

  • View in gallery

    In 2020, soil treatment did not have a consistent strong effect on at-harvest fruit quality. As in Fig. 2, to emphasize the tests for soil treatment effects, we reorganized the data presentation for at-harvest fruit quality of ‘Gala’ apple fruit, but for the second study year, 2020. For instance, if a treatment had a strong and consistent effect, significant differences would be concentrated in columns for that treatment; we did not observe this pattern. At harvest ‘Gala’ apple fruit quality from the 2020 harvest season. Values are means (n = 18) ± se for each rootstock genotype (RG) by soil treatment (ST). Significant differences from analysis of variance with the Tukey honest significant differences correction for multiple pairwise comparisons were performed, with results indicated via shading according to their P value threshold. zST = soil treatment; Ctl = control treatment; Fum = fumigation treatment; SM2 = seed meal (SM) application rate of 2.2 t·ha−1; SM4 = SM application rate of 4.4 t·ha−1. SM application consisted of a 1:1 mixture Brassica juncea/Sinapis alba. The fumigation treatment was an application of 1,3-dichloropropene-chloropicrion (Telone C-35). yRG = rootstock genotype; ‘Malling 26’ (‘M.26’); ‘Geneva 41’ (‘G.41’). xWeight (g); diameter (cm); starch index (1–6); Brix° = suspended solids; TA = titratable acidity; IEC = internal ethylene concentration (μL·L−1); Red % = red overcolor percent coverage; Red h° = red color hue angle; Red Chroma = red color chroma; Ground h° = background color hue angle; Ground Chroma = background color chroma; OMH = overall maximum hardness (N); M1 = maximum hardness region 1 (N); Qf = overall quality factor.

  • View in gallery

    Apple rootstock genotype has a greater influence on postharvest apple fruit quality than soil treatment. Similar to at-harvest data, after 10 weeks of cold storage in air the rootstock genotype still has a greater effect on fruit quality. Fruit quality changed largely as expected during the postharvest period, with at-harvest patterns persisting. Postharvest ‘Gala’ apple fruit quality after 10 weeks of cold storage from both the 2019 and 2020 harvest seasons is shown. Values are means (n = 18) ± se for each rootstock genotype (RG) by soil treatment (ST). Significant differences in pairwise t test results between RGs ‘Malling 26’ (‘M.26’) and ‘Geneva 41’ (‘G.41’) within each ST are indicated via shading according to their P value threshold. zST = soil treatment; Ctl = control treatment; Fum = fumigation treatment; SM2 = seed meal (SM) application rate of 2.2 t·ha−1; SM4 = SM application rate of 4.4 t·ha−1. SM application consisted of a 1:1 mixture Brassica juncea/Sinapis alba. The fumigation treatment was an application of 1,3-dichloropropene-chloropicrion (Telone C-35). yRG = rootstock genotype; ‘Malling 26’ (‘M.26’); ‘Geneva 41’ (‘G.41’). xWeight (g); diameter (cm); starch index (1–6); Brix° = suspended solids; TA = titratable acidity; IEC = internal ethylene concentration (μL·L−1); Red % = red overcolor percent coverage; Red h° = red color hue angle; Red Chroma = red color chroma; Ground h° = background color hue angle; Ground Chroma = background color chroma; OMH = overall maximum hardness (N); M1 = maximum hardness region 1 (N); Qf = overall quality factor.

  • View in gallery

    In 2019, soil treatment did not have a consistent strong effect on postharvest fruit quality. To emphasize the tests for soil treatment effects, we reorganized the data presentation for postharvest fruit quality of ‘Gala’ apple fruit in 2019 alone. For instance, if a treatment had a strong and consistent effect after 10 weeks of cold storage in air, significant differences would be concentrated in columns for that treatment; we did not observe this pattern. Values are means (n = 18) ± se for each rootstock genotype (RG) by soil treatment (ST). Significant differences from analysis of variance with the Tukey honest significant differences correction for multiple pairwise comparisons were performed, with results indicated via shading according to their P value threshold. zST = soil treatment; Ctl = control treatment; Fum = fumigation treatment; SM2 = seed meal (SM) application rate of 2.2 t·ha−1; SM4 = SM application rate of 4.4 t·ha−1. SM application consisted of a 1:1 mixture Brassica juncea/Sinapis alba. The fumigation treatment was an application of 1,3-dichloropropene-chloropicrion (Telone C-35). yRG = rootstock genotype; ‘Malling 26’ (‘M.26’); ‘Geneva 41’ (‘G.41’). xWeight (g); diameter (cm); starch index (1–6); Brix° = suspended solids; TA = titratable acidity; IEC = internal ethylene concentration (μL·L−1); Red % = red overcolor percent coverage; Red h° = red color hue angle; Red Chroma = red color chroma; Ground h° = background color hue angle; Ground Chroma = background color chroma; OMH = overall maximum hardness (N); M1 = maximum hardness region 1 (N); Qf = overall quality factor.

  • View in gallery

    In 2020, soil treatment did not have a consistent strong effect on postharvest fruit quality. To emphasize the tests for soil treatment effects, we reorganized the data presentation for postharvest fruit quality of ‘Gala’ apple fruit in 2020 alone. For instance, if a treatment had a strong and consistent effect after 10 weeks of cold storage in air, significant differences would be concentrated in columns for that treatment; we did not observe this pattern. Values are means (n = 18) ± se for each rootstock genotype (RG) by soil treatment (ST). Significant differences from analysis of variance with the Tukey honest significant differences correction for multiple pairwise comparisons were performed, with results indicated via shading according to their P value threshold. zST = soil treatment; Ctl = control treatment; Fum = fumigation treatment; SM2 = seed meal (SM) application rate of 2.2 t·ha−1; SM4 = SM application rate of 4.4 t·ha−1. SM application consisted of a 1:1 mixture Brassica juncea/Sinapis alba. The fumigation treatment was an application of 1,3-dichloropropene-chloropicrion (Telone C-35). yRG = rootstock genotype; RGs ‘Malling 26’ (‘M.26’) and ‘Geneva 41’ (‘G.41’). xWeight (g); diameter (cm); starch index (1–6); Brix° = suspended solids; TA = titratable acidity; IEC = internal ethylene concentration (μL·L−1); Red % = red overcolor percent coverage; Red h° = red color hue angle; Red Chroma = red color chroma; Ground h° = background color hue angle; Ground Chroma = background color chroma; OMH = overall maximum hardness (N); M1 = maximum hardness region 1 (N); Qf = overall quality factor.

  • View in gallery

    Map of tree establishment on 1 June 2016. This block is located within the Washington State University/United States Department of Agriculture-Agricultural Research Service Columbia View Research and Demonstration Orchard near East Wenatchee, WA (N 47° 37′ 33″, W 120° 13′ 31″). The map used here was adapted from Wang and Mazzola (2019). Background color indicates the type of soil amendment used. Each row has 4 soil amendment sections. Each soil amendment section was approximately 10.5 m in length and divided into two sections, one section was planted with five ‘Gala’ scion grafted onto rootstock genotype ‘Malling 26’ (‘M.26’), and the other section was planted with five ‘Gala’ scion grafted onto rootstock genotype ‘Geneva 41’ (‘G.41’). Each section contained 10 total trees. Within each row, a 1.5 m space separated each soil amendment section. Rows were spaced approximately 4.5 m apart. During the first two years of growth, trees were minimally managed using standard pesticide applications and trimmed to prevent limb breakage (M. Mazzola, personal communication). After the 2018 growing season, trees were managed according to standard commercial practices to optimize fruit quality.

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