Abstract
The genus Aronia Medik., also known as chokeberry, is a group of deciduous shrubs in the Rosaceae family, subtribe Malinae. The two commonly accepted black-fruited Aronia species are black chokeberry [Aronia melanocarpa (Michx.) Elliott] and aroniaberry [Aronia mitschurinii (A.K. Skvortsov & Maitul)]. The geographic range of wild A. melanocarpa is the Great Lakes region and the northeastern United States, with a southerly extension into the higher elevations of the Appalachian Mountains. Wild A. melanocarpa found in New England are diploids, whereas plants throughout the rest of the range are tetraploids. A. mitschurinii is a cultivated hybrid between ×Sorbaronia fallax (C.K.Schneid.) C.K.Schneid. and A. melanocarpa and exists as a tetraploid. There is currently limited diversity of Aronia genotypes in the ornamental and fruit industries, and many of the current cultivars are not adapted to the southern United States and similar environs with limited chilling to break winter dormancy. The goal of this study was to determine 1) the chilling requirements for A. mitschurinii ‘Viking’ and 2) the range of chilling requirements for wild A. melanocarpa genotypes from different geographic origins. Two experiments were conducted in which plants were subjected to various chilling accumulation treatments and then moved to a greenhouse for observation of budbreak and subsequent growth. Expt. 1 was conducted at the University of Maryland at Wye, MD, and focused solely on the commercial cultivar A. mitschurinii ‘Viking’. Outdoor, ambient fall and winter temperatures were used to achieve the chilling treatments. In Expt. 1, we determined the optimal chilling requirements for A. mitschurinii ‘Viking’ to be greater than 900 h using the single temperature model. Expt. 2 was conducted at the University of Connecticut and focused on wild genotypes, plus A. mitschurinii ‘Viking’. A fixed temperature cold room was used to achieve chilling treatments. In Expt. 2, we found A. melanocarpa genotypes from southern regions in the United States required chilling accumulation of 600 h (single temperature model), compared with genotypes from northern regions that required more than 900 h of chilling accumulation. Tetraploid A. melanocarpa required 900 h of chilling to break bud, but diploid A. melanocarpa required 1200 h of chilling to break bud. Expt. 2 confirmed the 900-h chilling requirement for A. mitschurinii ‘Viking’. For both experiments, the rate of budbreak and shoot growth was positively correlated with increasing amounts of chilling.
Aronia melanocarpa (Michx.) Elliott, commonly known as black chokeberry, are multistemmed deciduous shrubs belonging to the Rosaceae family, subtribe Malinae (Sun et al. 2018). Interest in Aronia has increased because their fruits contain high levels of polyphenolic compounds, primarily anthocyanins, and high antioxidant activity that is beneficial for human nutrition (Brand et al. 2017; Wu et al. 2004; Zheng and Wang 2003). Aronia species are also a valuable replacement for invasive exotic ornamental plants (Brand 2010) and are adaptable to a wide range of geographic regions. A. melanocarpa is native to North America and can easily be identified by the presence of ovate to obovate glabrous leaves and dark colored fruits in mid to late summer. A. melanocarpa are found as diploids (A. melanocarpa-2x) and tetraploids (A. melanocarpa-4x) in the wild and reproduce sexually and asexually via diplosporous apomixis, respectively (Mahoney et al. 2019). The base chromosome number for Aronia is n = 17 (Sax 1931). Most A. melanocarpa-2x are found in the northeastern United States, predominantly in the New England region (Brand 2010; Brand et al. 2022). A. melanocarpa-4x are found in the Northeast, primarily outside of New England, and span into southern Canada, the midwestern United States, the Great Lakes region, and southward into Appalachia (Brand 2010; Brand et al. 2022). A. melanocarpa-4x found across the southern-most parts of the range have distinct morphology and genetic profiles (Brand et al. 2022), and perhaps warrant re-classification as a distinct species. Another tetraploid Aronia species, used in fruit production, has been recognized as A. mitschurinii (A. mitschurinii-4x) (Skvortsov and Maitulina 1982; Skvortsov et al. 1983) and is the result of intergeneric hybridization between A. melanocarpa and Sorbus aucuparia (Leonard et al. 2013; Mahoney et al. 2018). Aronia fruit production is composed primarily of a single cultivar, A. mitschurinii ‘Viking’. Several other A. mitschurinii cultivars are reported, but these have been found to be exactly, or nearly, genetically identical to A. mitschurinii ‘Viking’ (Mahoney et al. 2018).
Cultivation of woody-temperate plants requires an adequate accumulation of chilling temperatures once dormancy is achieved to initiate growth in spring (Arora et al. 2003). These plants have evolved this critical period of dormancy, referred to as endodormancy, to minimize low temperature damage to vegetative and floral buds by delaying budbreak until warm temperatures return. This form of dormancy is typically initiated by low temperatures and short daylengths. However, a previous study has shown that some plants in the Rosaceae family are insensitive to photoperiod for dormancy induction (Heide and Prestrud 2005). After a period of chilling, endodormancy is broken and the plant is ready to initiate budbreak. It has been well documented that chilling requirements vary between species and genotypes from different geographical locations, but the exact biochemical and genetic mechanisms are still unknown (Campa and Ferreira 2018; Leida et al. 2012; Mehlenbacher 1991). The accumulation of chill units experienced by the plant is an important factor that determines when budbreak will occur.
The limited diversity of Aronia germplasm in fruit production and the ornamental landscape has prompted breeding efforts to focus on developing traits relating to disease pressure, fruit quality, and adaptability to changing climates. In the present study, we identify the chilling requirements for the commercial fruit type, A. mitschurinii ‘Viking’, and the different chilling requirements for budbreak in wild A. melanocarpa genotypes representing a wide geographic range.
Materials and Methods
Expt. 1: Maryland
Plant material and chilling treatments.
Expt. 1 was conducted in 2014/2015. A. mitschurinii ‘Viking’ rooted cuttings were established in 1-gallon pots with a peat-based substrate in May and were grown in a greenhouse for 4 months at the Wye Research and Education Center, Queenstown, MD (Table 1). Fifty plants were placed outside on Sep 1 to initiate dormancy and then receive chilling by exposure to natural outdoor cold temperatures. Average hourly outside ambient air temperature was recorded by a data logger weather station (CR1000 X; Campbell Scientific, Logan, UT, USA) ∼500 m from the plants.
Aronia germplasm used in chilling studies with geographic location of origin, ploidy level, and taxonomic group designation.
Randomly selected sets of eight plants of A. mitschurinii ‘Viking’ were moved into the greenhouse on 9, 16, 24, and 28 Dec 2014 and 5 and 21 Jan 2015 and were designated as sets one through six (Table 2). Greenhouse conditions were maintained at 23 °C under long-day (16 h) conditions using natural daylight that was extended with supplemental lighting.
Number of chill units accumulated in the Maryland study (Expt. 1) as calculated using three models.
Data collection and analysis.
Calculations for chill units began after dormant buds formed in Sep and the temperatures dropped below 12.8 °C. Three models were used to calculate accumulated chill units (Table 2). The single temperature model (model 1) assigned one chill unit for every hour below 7 °C (Weinberger 1950) and the dual temperature model (model 2) assigned one chill unit for every hour between 0 °C and 7 °C (Byrne and Bacon 1992). The Utah model (model 3) assigns one chill unit for every hour between 2.2 °C and 8.9 °C and one-half (0.5) chill unit for every hour between 1.7 °C and 2.2 °C or 8.9 °C and 12.8 °C (Richardson et al. 1974). No chill units are assigned between 12.8 °C and 15.6 °C and below 1.7 °C. One-half (0.5) chill unit is subtracted from the accumulation for every hour between 15.6 °C and 18.3 °C. One chill unit is subtracted from the accumulation for every hour above 18.3 °C. Plants were observed weekly in the greenhouse for bud swell and terminal budbreak, with terminal budbreak characterizing chilling requirements being met. Plants were allowed to proceed to full expansion of shoots, leaves, and flowers over a period of 11 weeks.
The experiment was designed as a completely randomized design with eight replicates per chilling treatment. Pairwise multiple comparisons among proportions were performed with the R package rstatix (version 0.4.0) using the pairwise_fisher_test function (Kassambara 2020).
Expt. 2: Connecticut
Plant material and chilling treatments.
In total, 15 different genotypes (Table 1; Fig. 1) including four genotypes of A. melanocarpa-2x, six genotypes of A. melanocarpa-4x, four genotypes of A. melanocarpaS-4x, and one genotype of A. mitschurinii-4x were used. Cuttings were collected on 20 Jun 2018 from the University of Connecticut Aronia germplasm collection in Storrs, CT, USA, treated with indole-3-butyric acid rooting hormone (Hormodin 2; OHP Inc., Mainland, PA, USA) and rooted under intermittent mist in 6.5 cm × 6.5 cm × 8.8 cm containers containing 1 sphagnum peatmoss:1 medium horticultural grade vermiculite:1 medium perlite. Rooted cuttings were acclimated to greenhouse conditions and then moved outdoors into cold frames for the remainder of the growing season. Plants were fertigated once a week with a soluble fertilizer (Peters 20N–8.7P–16.6K; Scotts, Marysville, OH, USA) providing 200 ppm nitrogen (N) once they were rooted and up until 1 Oct 2018. Plants were allowed to go dormant in response to natural photoperiod and cold temperatures.
Map of Aronia germplasm used in the Connecticut study showing geographic distribution of taxonomic groups and accessions.
Citation: HortScience 58, 9; 10.21273/HORTSCI17278-23
The Aronia genotypes were tested for chilling requirements by placing dormant rooted cuttings into a walk-in cooler with a set point temperature of constant 6 °C and cool white fluorescent lighting (50 μmol⋅m−2⋅s−1) with a short-day photoperiod of 8 h on 24 Oct 2018. Five different chilling treatments were achieved by providing 0 (no chilling), 300, 600, 900, and 1200 h of duration in the walk-in cooler. After exposure to chilling treatments, a subset of rooted cutting accessions selected at random, was moved to a warm greenhouse. The experimental unit was a single plant for A. mitschurinii-4x, four plants (one plant per 2x accession) for A. melanocarpa-2x, six plants (one plant per 4x accession) for A. melanocarpa-4x, and four plants (one plant per southern 4x accession) for A. melanocarpaS-4x. In the greenhouse, experimental units were arranged in a randomized complete block with 10 replications. Each time plants were brought out of the cooler and added to the greenhouse population they were all rerandomized. The greenhouse had set points of 21 °C/17 °C day/night and long-day (16 h) conditions using natural daylight that was extended with 400 W high-pressure sodium lamps (P. L. Light Systems, Beamsville, Ontario, Canada). In the greenhouse, plants were fertigated once a week with a soluble fertilizer (Peters 20N–8.7P–16.6K; Scotts) providing 200 ppm nitrogen (N).
Data collection and analysis.
Dormancy break data were collected for each chilling treatment at 15 d, 30 d, 60 d, and 120 d following placement in warm greenhouse conditions. Number of buds present on each plant, number of buds that broke dormancy, total shoot length, and average shoot length were recorded at each collection time. Buds were considered to have broken when 2 mm of extended tissue was visible. Significance was determined by analysis of variance and differences between means were compared by Fisher’s least significance difference test using the R package agricolae (version 1.3–1) (de Mendiburu 2019).
Results
Expt. 1: Maryland.
Chill unit calculations began on 2 Oct 2014. The first set of plants had accumulated 586 (model 1), 501 (model 2), and 368 (model 3) chill units (Table 2). Apart from bud swell, no plants from set 1 broke dormancy throughout the entire observation period. The second set of plants had accumulated 736 (model 1), 648 (model 2), and 497 (model 3) chill units and bud swell was observed from 14 d to 28 d after dormancy break initiation (DBI). One plant had terminal budbreak at 49 d, but no other plants had broken terminal bud by the end of the study on day 77 (Fig. 2). The third set of plants had accumulated 888 (model 1), 761 (model 2), and 591 (model 3) chill units, and bud swelling was noted in most plants at 14 d after DBI. Three plants had broken terminal buds at 35 d and one more plant broke a terminal bud at 56 d (Fig. 2). By the end of data collection, half of the plants had come fully out of dormancy. The fourth set of plants had accumulated 929 (model 1), 800 (model 2), and 643 (model 3) chill units (Table 2) and after 2 weeks in warmth, bud swell started to occur on four of the plants. Two plants had broken terminal buds by 28 d after DBI. One additional plant had broken terminal buds by day 35, and by day 56 another had broken terminal buds (Fig. 2). The fifth set of plants had accumulated 1087 (model 1), 922 (model 2), and 746 (model 3) chill units. Individual plants in the fifth set broke terminal buds on days 21, 28, 42, 49, 56, and 77, so that all plants had broken dormancy by the end of the study (Fig. 2). The final set of plants had accumulated 1470 (model 1), 1065 (model 2), and 808 (model 3) chill units. One plant broke terminal buds on day 21 and a second plant broke terminal buds on day 28, but no other plants broke terminal buds by the end of the study on day 77 (Fig. 2). At 77 d after DBI, significant differences were observed between plants in set 1 and set 5 (P = 0.0022), and between plants in set 2 and set 5 (P = 0.0047) using Fisher’s pairwise exact test. All plants in set 5 exhibited budbreak indicating that this treatment had optimized chilling relative to the other cold treatments. Compared with set 5, set 3 exhibited decreased budbreak, indicating this treatment had received insufficient chilling time (Fig. 3).
Aronia mitschurinii ‘Viking’ plants breaking terminal buds in the Maryland study (Expt. 1) over 77 d after dormancy break initiation (DBI) following exposure to increasing accumulated chilling hours as calculated by the single temperature (model 1), dual temperature (model 2), and Utah chill models (model 3).
Citation: HortScience 58, 9; 10.21273/HORTSCI17278-23
Appearance of Aronia mitschurinii ‘Viking’ plants in Maryland study (Expt. 1) that (A) received an insufficient amount of chilling and exhibited poor budbreak and shoot grow out in response to warm greenhouse conditions in comparison with plants that (B) received sufficient chilling and are exhibiting strong budbreak and shoot grow out in response to warm greenhouse conditions. Plants in (A) received 736, 648, or 497 chill units based on the single temperature, dual temperature, and Utah models. Plants in (B) received 1087, 922, and 746 chill units based on the same models.
Citation: HortScience 58, 9; 10.21273/HORTSCI17278-23
Expt. 2: Connecticut.
For plants receiving no chilling, the first budbreak was observed 60 d after DBI in the A. melanocarpaS-4x group. Ames 33077 was the only accession in the A. melanocarpaS-4x group to begin budbreak after 60 d. By 90 d after DBI, A. melanocarpaS-4x accessions had a significantly (P < 0.001) higher percentage of budbreak per plant than the other taxonomic groups (Fig. 4). Every taxonomic group had budbreak at 120 d even when they received no chilling; however, the vigor of budbreak and length of shoot extension was not sufficient for normal plant development. For plants receiving 300 h of chilling, first budbreak was observed at 60 d after DBI for all accessions in the A. melanocarpaS-4x group. Other taxonomic groups exhibited budbreak at 120 d after DBI (Fig. 4). The rate of budbreak and shoot development for plants receiving 300 h of chilling was also inadequate for normal plant growth. At 120 d, the A. melanocarpaS-4x group had 25.0% budbreak and produced shoots with an average length of 12 mm. All other taxonomic groups had significantly less budbreak and shoot extension (Fig. 4). Plants in the A. melanocarpaS-4x and A. melanocarpa-4x groups that received 600 h of chilling began to break buds at 15 d after DBI (Fig. 4). At 60 d after DBI, A. melanocarpa-2x had significantly less budbreak than A. melanocarpaS-4x (P < 0.001), but similar budbreak (P = 0.056) as A. melanocarpa-4x (Fig. 5). A. mitschurinii-4x receiving 600 h of chilling did not begin to break bud until 120 d after DBI and had an average budbreak of 27% (Fig. 4). For plants that received 900 h of chilling, only the A. melanocarpaS-4x group exhibited budbreak at 15 d after DBI (Fig. 4). A. melanocarpa-2x and A. melanocarpa-4x began budbreak at 30 d after DBI, with A. mitschurinii-4x exhibiting budbreak by 60 d after DBI. A. mitschurinii-4x produced greater average shoot length and total shoot length than all other taxonomic groups (P < 0.001) but percent budbreak was only significantly different from that of A. melanocarpa-2x (Fig. 5). All groups receiving 900 h of chilling had 36% to 48% budbreak and average shoot length of 24 to 132 mm at 120 d after DBI. Although all plants receiving 1200 h of chilling exhibited budbreak at 15 d after DBI, A. mitschurinii-4x produced the most budbreak compared with the other taxonomic groups (P = 0.0014) (Fig. 4). At 120 d after DBI, A. mitschurinii-4x had 87% budbreak and an average shoot length of 96 mm, while other groups had ∼61% budbreak with an average shoot length of between 46 and 63 mm (Fig. 4). A. mitschurinii-4x that received 900 h of chilling (Fig. 5) broke just slightly more than half as many buds (∼33%) as plants that received 1200 h of chilling (∼60%). Plants that received 900 h or 1200 h of chilling produced similar amounts of total shoot length at ∼90 mm (Fig. 5). However, plants that received 900 h of chilling produced shoots with an average length of 100 mm, whereas plants that received 1200 h of chilling produced shoots with an average length of only 60 mm. Figure 6 illustrates the amount of budbreak and shoot growth exhibited by plants from different Aronia taxonomic groups in response to increasing chilling hours at 6 °C following 60 d of growth in a warm greenhouse.
The total shoot length, average shoot length, and percent budbreak per plant over the course of 120 d following dormancy break initiation for different taxonomic groups of Aronia exposed to increasing accumulated chilling hours at 6 °C. Bars represent standard error of the mean.
Citation: HortScience 58, 9; 10.21273/HORTSCI17278-23
The total shoot length, average shoot length, and percent budbreak per plant at 60 d after dormancy break initiation for different Aronia taxonomic groups in response to increasing accumulated chilling hours at 6 °C. Bars with the same letter within each chill hour accumulation treatment did not differ significantly according to Fisher’s least significant difference test (P < 0.05).
Citation: HortScience 58, 9; 10.21273/HORTSCI17278-23
Representative plants of four Aronia taxonomic groups exposed to increasing accumulated chilling hours at 6 °C showing degree of budbreak and shoot extension at 60 d after dormancy break initiation (bar = 60 mm).
Citation: HortScience 58, 9; 10.21273/HORTSCI17278-23
Discussion
Fulfilling chilling requirements is an important biological process to consider when selecting genotypes for a particular region (Ruiz et al. 2007). Previous estimates, based on observation of A. mitschurinii-4x in grower orchards in more southern parts of the United States, suggest that this species requires between 800 and 1000 chill hours before budbreak can occur (Everhart 2011). These estimates for chilling requirements of A. mitschurinii-4x have not previously been confirmed with research studies. We found the minimum chill unit requirement for A. mitschurinii-4x to be 900 h using a single temperature model. Additional accumulation of chilling to 1200 h produced more complete budbreak with enhanced growth and development of shoots and flowering (Fig. 6). Plants receiving only 900 h of chilling broke fewer buds, which developed into longer shoots, than plants that received 1200 h of chilling and produced greater budbreak and more shoots with moderate length. It is likely that plants receiving only the minimum required chilling over repeated dormancy and growth cycles will develop different habits and substandard fruit crops in comparison with plants receiving annual optimum chilling. We recommend that fruit producers seek to grow A. mitschurinii-4x only if their orchard location regularly receives more than 1000 h of dormant chilling. US Department of Agriculture (USDA) Hardiness Zone 7a (USDA Plant Hardiness Zone Map 2012) is probably the warmest area a fruit grower can be in and expect to have dependable success with A. mitschurinii-4x because of insufficient chilling.
Sorbus aucuparia L., one of the parents involved in the creation of the intergeneric hybrid A. mitschurinii-4x, has been reported to have a cold requirement of 750 h at temperatures below 7 °C (Kronenberg 1994). There are no reports of research studying the chilling requirements of wild forms of A. melanocarpa, the other parent of A. mitschurinii-4x, but our findings show that most forms of A. melanocarpa require a minimum of 900 h of chilling to break bud. Furthermore, budbreak of wild A. melanocarpa is enhanced with chilling hours closer to 1200 h. Given the parental species chilling needs for dormancy release, it is not surprising that A. mitschurinii-4x has a minimal chilling requirement of 900 h and an optimum chilling requirement of closer to 1200 h.
Substantial differences in dormancy release in response to chilling hours were observed among the three wild taxonomic entities (northern diploid, northern tetraploid, and southern tetraploid) of A. melanocarpa. Diploids, whose geographic distribution is essentially limited to New England, produced only weak budbreak following 900 h of chilling and demonstrated a more complete requirement of 1200 h of chilling to break bud vigorously and uniformly. Northern tetraploids, which are primarily from Great Lakes states in the northern United States, broke bud reasonably well after 900 h of chilling, but showed more complete and vigorous budbreak after 1200 h of chilling. Southern tetraploids, found in Missouri, Tennessee, Virginia, and possibly other southern states, produced some budbreak with as little as 300 h of chilling and exhibited strong budbreak following 600 h of chilling. Only modest enhancements in budbreak were realized when A. melanocarpaS-4x plants received 900 h or 1200 h of chilling.
Ploidy was related to chilling requirement with diploid A. melanocarpa from northern locations needing more chilling than tetraploids from northern locations to break bud dormancy well. In kiwifruit cultivars of diploid, tetraploid, and hexaploidy ploidy levels, an opposite relationship was found. Chilling requirements for diploid cultivars were significantly lower than for hexaploid cultivars, with tetraploid cultivars being intermediate (Zhao et al. 2017). The mechanisms whereby ploidy level can affect shoot and bud dormancy in woody plants remains unclear and has been studied very little. Because diploid A. melanocarpa are found primarily in New England, it may be that the seasonal weather conditions in that region make plants requiring longer chilling periods more successful than plants with shorter chilling requirements.
There was a clear correlation between geographic origin and chilling requirements for black-fruited Aronia accessions, where plants originating from southern latitudes required significantly less chilling to break bud than plants originating from northern latitudes. A similar correlation has been observed for Acer rubrum L., where plants from Florida required no chilling to break bud, but accessions from New York and Pennsylvania required at least 1 month of chilling to break bud (Perry and Wu 1960). Styrax americanus Lam. was also shown to exhibit different chilling requirements depending on geographic origin of the germplasm (Lenahan et al. 2010). Plants from Florida had the lowest chilling requirement of 351 chilling hours to achieve budbreak, whereas those from northern Illinois needed 520 chilling hours to break bud. Longer chilling requirements for northern ecotypes than for southern ecotypes also have been reported for Liquidambar styraciflua L. (Farmer 1968) and Picea A. Dietr. species (Nienstaedt 1967). In contrast, longer chilling requirements in southern ecotypes than in northern ecotypes were found in several Betula L. species (Myking and Heide 1995; Sharik and Barnes 1976). A similar relationship between geographic location and chilling needs was shown for wild grape (Vitis L.) species, in which those from northern latitudes required less cold than those from southern latitudes to break bud (Londo and Johnson 2014). Such differences may depend on the specific latitudinal trends in climatic factors to which various species have been adapted (Myking and Heide 1995).
Insufficient chilling in much of the southern United States makes A. mitschurinii-4x a nonviable fruit crop in those areas. To expand Aronia production farther south, new cultivars need to be developed that require less chilling to break dormancy. Identification of A. melanocarpaS-4x genotypes that require significantly less chilling to break dormancy than most A. melanocarpa suggest that it may be possible to incorporate this southern germplasm into an Aronia breeding program to develop low chill requiring A. mitschurinii cultivars that require reduced chilling units to support fruit production in the southern United States. In addition, southern tetraploid genotypes can be used directly to expand the range southward where A. melanocarpa can be grown successfully as an ornamental landscape shrub.
This is the first study to investigate and report the chilling requirements for some Aronia taxonomic groups. This information will be useful in identifying regions that are most suitable for Aronia production using current Aronia cultivars. Identification of the chilling requirements of different Aronia germplasm will inform breeding efforts aimed at expanding the geographic areas where Aronia can be successfully grown as a fruit crop and ornamental plant.
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