by Daniel J. Donahue 1*, Gemma Reig Córdoba 2, Sarah E. Elone 1, Anna E. Wallis 3 and Michael R. Basedow 4
1 Eastern New York Commercial Horticulture Program, Cornell Cooperative Extension, Cornell University, 3357 Route 9W, Highland, NY 12528, USA
2 IRTA Fruitcentre, Tree Fruit Production, PCiTAL, Park of Gardeny, Fruitcentre Building, 25003 Lleida, Spain
3 Cooperative Extension, Michigan State University, 775 Ball Ave NE, Grand Rapids, MI 49503, USA
4 Eastern New York Commercial Horticulture Program, Cornell Cooperative Extension, Cornell University, 6064 Route 22 Suite 5, Plattsburgh, NY 12901, USA
* Author to whom correspondence should be addressed.
The following is a summary of the full article published May 2021 in the MDPI open-access journal “Plants”. The full text document along with all figures and tables can be accessed by clicking on the link here or typing the following URL into your web browser: https://www.mdpi.com/2223-7747/10/5/983/htm#
At a Glance, What We Learned from this Study
- Bud 9 offers superior “real-world” bitter pit performance in Eastern New York (ENY) commercial orchards.
- Looking towards future ‘Honeycrisp’ plantings, the real-world bitter pit performance of the rootstock should be a major factor for grower consideration.
- Geographic region influences the extent of bitter pit symptom expression.
- Within the range of acceptable maturity standards, later spot picks offer improved bitter pit performance in storage.
- Yes, up to a point, larger fruits express more bitter pit. However, within our commonly marketed count sizes, the “size effect” is not especially significant and is actually neutral for fruits produced on B.9.
- Many factors other than absolute mineral content influence the expression of bitter pit symptoms.
- The results of our study both simplify and complicate efforts to develop bitter pit prediction protocols and models.
Study Objective and Methods
The aim of this study was to broadly examine potential contributors to the large variation observed in the rate of bitter pit incidence on ‘Honeycrisp’ in the New York State climatic environment. We focused on rootstock and region, analyzing weather, soil, horticultural and fruit quality variables, using multivariate and binomial distribution analysis techniques. Our goal was to describe as much of the biological and abiotic world that our 6-tree experimental units were expected to thrive in while producing marketable fruit in commercial settings.
In the course of this work, we evaluated a high number of parameters as possible indicators of BP incidence, including weather and soil traits, horticultural and fruit quality characteristics, through the perspective of region and rootstock choice, by conducting a detailed survey of 34 ‘Honeycrisp’ blocks distributed across two growing regions in Eastern NY, which at the end we included 30 blocks in our analysis. Data were collected on 43 orchard parameters with a total of 13,770 apples individually rated and tracked through storage for selected fruit quality parameters whenever practical. Continuous, binomial, parametric and non-parametric statistical analyses were applied as appropriate. The authors can say with confidence that the commercial producers who donated their orchards to this study were among the most skilled in New York State, with well-managed ‘Honeycrisp’ plantings.
Results and Discussion
Commonly Considered Horticultural Parameters
‘Honeycrisp’ trees on B.9 rootstock were smaller but with comparable terminal shoot growth when compared to those on M.26 and M.9 rootstocks. B.9 fruits, which had similar fruit size to M.26 and M.9 and had good fruit quality at harvest and after storage, were much less likely to express bitter pit symptoms compared to M.9 and M.26 rootstocks.
Regional and Rootstock Effects on Bitter Pit
Regional and local environmental and soil conditions must be taken in consideration when planting a new orchard and may be significant contributors to BP predisposition. To the best of our knowledge, this is the first study evaluating the region effect on the occurrence of BP. After three years and comparing the two regions, we found that, in general, ‘Honeycrisp’ orchards from the HV region presented high BP incidence relative to the Champlain Valley. This region received more rain and experienced higher temperatures over the study period, which may explain partially the difference in BP.
Rootstock choice is one of the most critical elements of any apple orchard to provide sufficient growth control, enhanced precocity, higher yield, improved adaptability to environmental conditions, and better fruit quality . In addition to effects on these traits, apple rootstocks have a diverse influence on the nutritional status of the tree canopy, are implicated in the physiology of BP and, therefore, can affect the occurrence of BP [2,3,4], as it is demonstrated in our results. However, the BP response to tissue mineral status is variable depending on the rootstock and the region where it is planted. As a result, the occurrence of BP can be more or less intense or absent even as local tree tissue mineral measurements suggest otherwise.
We evaluated three of the most popular rootstocks used in high-density apple orchards in New York State: B.9, M.26 and M.9 clones . Among them, fruits from ‘Honeycrisp’ grafted on M.26 were slightly more susceptible to BP than those from M.9 clones and much more susceptible than B.9. In agreement with Lordan et al. , B.9 rootstocks had a much lower incidence of BP compared to M.26 and M.9 clones, even in the very dry year of 2016. In general, B.9 BP incidence values did not differ significantly among years by region, even when both regions were evaluated together. Kim and Ko  reported that BP is more intensive on moderate, vigorous rootstocks compared to less vigorous rootstocks, which is consistent with our results, as M.26 is the most vigorous rootstock in terms of TCSA evaluated in this study.
Shoot Growth Effects on Bitter Pit
Terminal shoot extension (ALTS) was a poor indicator of vigor and BP incidence as ALTS was very similar between the three rootstocks while BP differed significantly.
Nutrient Status Effects on Bitter Pit
In terms of nutrient status, region and rootstock had a significant effect on some of these traits, results that were somewhat expected. Other authors have also reported that region and rootstock can affect similar horticultural traits under Hudson Valley and Champlain Valley climatic conditions for ‘Gala’, ‘Fuji’ and ‘Honeycrisp’ [6,1,4]. In this study, the most vigorous rootstock, M.26, had higher leaf K/Ca, Mg/Ca and B/Ca ratios, leaf K, and peel B, but lower leaf Ca, Mn, and P values as compared to B.9 and M.9 clones.
Between regions, ‘Honeycrisp’ orchards, despite showing significant differences, some of these nutritional traits were not correlated to BP incidence after a period of refrigerated storage. ‘Honeycrisp’ fruits from CV orchards tended to have less BP incidence after storage (less than 10%) compared to those from HV. This lower BP value may explain the lower number of correlations with the horticultural traits, as well as the higher BP incidence values of M.26 orchards from HV could explain the higher number of significant correlations with horticultural traits compared to those from CV region.
Little correlation was found between BP incidence after storage on ‘Honeycrisp’ fruits from B.9 in terms of nutrient status, TCSA, peel Mg/Ca and peel Ca, whereas more significant correlations were found in fruit from the M.26 and M.9 clones, mainly the peel minerals. The lower BP incidence values from B.9 fruits could explain the lack of correlations compared to M.26 and M.9 clone rootstocks. These two rootstocks had some correlations in common, such as peel K/Ca, peel Mg/Ca, peel B/Ca, peel B, peel Ca, peel K and peel P, but M.9 clone rootstocks had higher values.
Recent studies have shown that BP, a Ca2+-related deficiency disorder, is not necessarily related to low Ca2+ concentration in fruit tissue in a “global” sense. In fact, chemical and X-ray analysis have shown that apple fruit tissue with visual Ca2+ deficiency symptoms had higher Ca2+ concentration than healthy fruit tissue . Most Ca2+ in fruit tissue, between 60 and 75%, is bound to the cell wall. More Ca2+ binding to the cell wall is consistent with the finding that BP-damaged tissues have more Ca2+ than the surrounding healthy tissues [8,9]. In agreement with this statement and previous studies [3,10], we found a high and negative correlation between peel Ca2+ concentration and BP incidence after storage for all three rootstock categories and two regions.
Fruit Quality Trait Effects on Bitter Pit
Fruit quality traits were also affected by region and rootstock, in agreement with previous rootstocks studies performed in ‘Gala’, ‘Fuji’, ‘Honeycrisp’ and ‘Red Delicious’ under Hudson Valley and Champlain Valley climatic conditions [6,1,4,11]. Both regions (CV and HV) had similar correlations between fruit dimensions and BP incidence after storage, despite showing significant differences on these traits. However, blush only correlated with BP on those ‘Honeycrisp’ from CV. BP incidence after storage had few and inconsistent correlations with fruit dimensions and fruit quality traits when rootstocks were compared. ‘Honeycrisp’ fruits from M.26 rootstock, which had in general smaller FD because they were more elongated but similar FW to B.9 and M.9 clones, presented a moderate positive correlation with BP incidence after storage on these three parameters, and a medium negative correlation with blush. In contrast, B.9 did not present any correlation on the same traits, while M.9 clones did in FD and FW, perhaps this finding is associated with lower levels of BP and less variability in the B.9 orchards. A similar trend was observed regionally for B.9.
Effect of Pick Timing on Bitter Pit Incidence
‘Honeycrisp’ fruits were harvested at optimum commercial harvest quality at each of the three weekly picking times. Minor fruit quality and maturity differences between picks at harvest were found but considered to be commercially acceptable for storage and marketing purposes. BP incidence at the time of harvest was relatively low and varied only slightly by pick with the pick 3 (last pick) apples expressing slightly more BP (Figure 2A). It would be unlikely for a commercial producer to observe the slight uptick in BP in the field. In contrast, BP incidence after storage showed a significant decreasing trend in each of the later picks in the HV, while in the lower BP environment of the CV, picks 2 and 3 were found to be similar, and lower than pick 1 (Figure 2B).
‘Honeycrisp’ fruits picked earlier were firmer, smaller, with more red blush and presented higher BP in storage. Therefore, in agreement with Prange et al. , BP is more severe in early-picked than in later-picked apples. However, there may be an optimum stage of fruit maturity (or harvest date) for ‘Honeycrisp’ when fruit are of sufficient size and color to meet market requirements while minimizing the risk of manifesting BP, especially if the fruit are >250 g in size. Our study did not attempt to specifically evaluate that possibility. We closely adhered to commonly accepted commercial quality standards. In any case there may not be much room available to adjust harvest dates and maintain a balance of quality factors acceptable to the marketplace.
Fruit Size and Bitter Pit Incidence
Increasing fruit size has been associated with increased BP incidence . The relationship was further defined by Reid and Kalcsits  in a water relations study where fruit size was categorized into four classes based on diameter, with BP incidence effectively doubling between the 80–90 mm and over 90 mm categories. Our study takes this approach a step further, with the use of ten commercial weight categories in the range of 48 count (largest) down to 140 count (smallest) based on common marketing practice (Figure 3). For all storage fruit in this study the frequency distribution of across the ten categories approximated the bell shape of a normal distribution with the top of the “bell” flattened (data not shown), with 92% of the fruit falling into count categories 56 to 113. For all three rootstocks, fruit in the categories 48 and 56 were the most susceptible to BP. While our categories were based on weight ranges, our fruit diameter data shows that 48 count apples averaged 94.1 mm and 56 count apples averaged 89.3 mm, both categories roughly equivalent to the largest size category described in the Reid and Kalcsits  study which also experienced an elevated incidence of BP. The relationships start to change by rootstock as we move into the more commonly marketed size categories. Fruit produced on B.9 had a relatively neutral relationship of BP to size in the range from 64 to 140 as the BP incidence curve flattened and oscillated around a mean of 11.2% incidence (Figure 3B). Fruit produced on M.9 demonstrated a decline in BP incidence with decreasing size, with incidence falling from 29.2% (64 count) to 13.3% (113 count) (Figure 3D). Fruit produced on M.26 demonstrated the most severe relationship falling from 40.6% to 14.6% over the same count size range (Figure 3C). There are orchard management implications associated with these findings. As much as the industry recognizes that larger fruit have more bitter pit, as a practical matter the first priority of a properly managed crop load reduction program is to produce fruit in marketable sizes, and then facilitate adequate return bloom to avoid biennial bearing. Minimizing the production of 48 and 56 count apples will have a positive effect on orchard financial returns for all rootstocks represented in this study. Beyond that, a shift in frequency distribution to smaller fruit is not likely to help in a B.9 orchard and will only slightly reduce the average BP incidence in M.9 clone and M.26 orchards.
The Complexity of Bitter Pit Prediction Modeling
While BP incidence has been related to individual mineral element concentrations and ratios of mineral pairs in many apple studies, one should not underestimate the complex environment that the roots (soil type, soil pH, water availability, soil moisture, etc.), and the scion (rainfall, light intensity, crop load, heat unit accumulation) operate in, in conjunction with the final fruit traits influence by producer management practices during the course of the dormant and growing seasons. For this reason, we pooled together all the traits evaluated in this study, except for CL, which was not evaluated in 2018, to identify the PLS prediction model on BP for each region and each rootstock based on the NIPALS algorithm.
Based on the results, the PLS prediction model for each region (CV and HV) and each rootstock (B.9, M.26 and M.9 clone) showed a different threshold of variables correlated to BP, described above for each PLS prediction model (Figure 4). However, comparing all PLS analysis, only seven VIP variables were in common, peel K/Ca, peel Mg/Ca, and peel B/Ca ratios, peel Ca, FD, L/FD, and FW, showing the great variability found in this study. It is also interesting to point out that none of the environmental variables and soil variables evaluated in this study were VIP variables in common among rootstocks or between regions. The 34 orchards evaluated in this study over three years represent a wide range of these variables, therefore, these results could help to emphasize their influence on BP incidence when taking in consideration each rootstock and each region as a single unit to evaluate.
Summary and Conclusions
The results of this work have the potential for a dramatic impact on commercial management and mitigation of BP in ‘Honeycrisp’ production. In order to facilitate real-time management changes, producers and marketers need practical tools and proven horticultural practices that mitigate bitter pit incidence and reduce storage decision risk. Bitter pit prediction models are currently in various stages of development, validation, and commercial implementation [15,16,17] with all three taking different approaches to meet the same goal of reliable pre-harvest prediction of ‘Honeycrisp’ fruit BP performance in storage. Recommended approaches should be those that are simple to implement at a low cost to the producer. However, the large number of variables suggests that simple and commercially achievable models consisting of 1–3 variables will always be lacking in absolute accuracy. Fortunately for practical implementation within the apple industry, accuracy thresholds for commercial implementation are more tolerant of error than those considered acceptable in academic settings. The goal is to provide effective storage management guidance which ultimately protects the producer from making the unprofitable decision to store fruit from an orchard that turns out to suffer substantial losses to BP months later.
Not all traits evaluated individually correlated significatively with bitter pit incidence after a period in storage. Depending on rootstock and region, the correlation could be significant in one situation, with no correlation at all in another. In this study, peel Mg/Ca ratio and peel Ca correlated with BP for all three rootstocks, with the strongest correlations associated with the M.9 clones. These same traits correlated with BP for both regions. Pick timing had a significant influence on BP incidence following storage, with later picks offering better bitter pit storage performance. While excessively large fruits, those in the 48 and 56 count size categories, were found to be highly susceptible to BP regardless of rootstock, B.9 BP fruit susceptibility for lesser sizes was found to be size neutral. A PLSR prediction model for each rootstock and each region showed that different variables correlated to BP depending on the situation.
We suggest that the BP performance of a rootstock should be a major consideration when choosing a rootstock for a new ‘Honeycrisp’ orchard in New York State and likely elsewhere as well. Unfortunately, data beyond anecdotal observations is difficult to find, and considering the variability found in this study, likely to be highly unreliable. We suggest that rootstocks newly introduced to the commercial market should be tested for BP performance during the developmental phase and before being recommended for widespread use with ‘Honeycrisp”, beyond the scope of modest producer test plantings.
In a more basic sense, these results could also suggest that in addition to the variables considered in this study, and commonly studied in others, there are other, less studied factors or triggers (genetic, histological, hormonal, abiotic stress situations, etc.) that can influence the physical expression of BP symptoms. With that said, identifying and understanding these factors may help to uncover the mechanism within the tree associated with the fruit, maintaining an adequate supply of calcium cations in the vicinity of groups of cells, making sure that they are available at the appropriate time, and what factors or combinations of factors influence the effectiveness of this calcium delivery mechanism, if possible.
The authors wish to acknowledge the efforts and in-kind contributions of all who collaborated with us towards the successful implementation of this project. Thank you to the Cornell Nutrition Analysis Laboratory, the Cornell Hudson Valley Research Laboratory, The Cornell Cooperative Extension Eastern New York Commercial Horticulture Program, and the 13 Eastern New York State apple producers (Table 1) for their contribution of laboratory and cold storage space, orchard sites, and substantial donations of experimental fruit. A special thank you to the many people who have helped our team by providing valuable guidance and insight including but not limited to Michael Rutzke, Christopher Watkins, Lailiang Cheng, Yousef Al Shoffe, Srdan Acimovic, Andy Galimberti, Sarah Tobin, Dana Acimovic, and Jeff Alicandro. Funding was provided by the New York State Department of Agriculture and Markets Apple Research and Development Program.
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