Towards Broader Adaptability of North American Deciduous Azaleas Alexander Q. Susko, James M. Bradeen, and Stan C. Hokanson

orth American deciduous azaleas have and many shades in between, providing tremen- long been adored by horticulturists. dous spring and summer interest in the garden. NThese plants, which belong to the Quickly recognized for their horticultural merit, genus Rhododendron sect. [section] Pentan- North American deciduous azaleas piqued the thera, comprise 15 species distributed from interest of plant collectors upon their discovery Texas to Florida, extending northwards to and continue to be widely lauded by gardeners southern Maine, and with one species occurring today. This has led to a proliferation of cultivars in mountainous areas of Oregon and California. and interspecific hybrids that provide a beauti- These species display a wide range of flower ful floral display every year both in gardens and color, from pure white to deep orange, pink, in the wild (Azalea Society of America 2016). WILLIAM (NED) FRIEDMAN

As a common name, “rhododendron” usually refers to large evergreen shrubs whose flowers have ten stamens, such as this elepidote cultivar ‘Album Grandiflorum’ (accession 22810-A) growing in the Arnold Arboretum’s Rhododendron Dell. 16 Arnoldia 74/2 • October 2016

Over 240 unique accessions of Rhododendron sect. Pentanthera exist at the Arnold Arbore- tum including many interspecific hybrids, vari- The Linnaean system classifies organisms into ous cultivars, and 12 of the 15 deciduous azalea increasingly narrow groups until reaching the species native to North America (Table 1). The individual species level. Classification (to the accessions at the Arnold Arboretum have ori- section level) for the North American deciduous gins in a wide range of environments and could azaleas is shown here (US-GRIN 2016). contain many useful adaptations to common abiotic (non-living) stressors. This collection Kingdom...... Plantae thus represents a valuable asset to woody plant Order...... Ericales researchers who seek to understand the adap- tive potential of these plants to better benefit Family...... Ericaceae gardeners and ecosystems alike. Genus...... Rhododendron Those who have spent any time researching Subgenus...... Hymenanthes azalea species or cultivars quickly discover a Section...... Pentanthera confusing naming system. Azaleas are actually a now informal designation within the genus Rhododendron, a large genus of 1,024 species in the heath family (Ericaceae) with a distribution spanning across the north- ern hemisphere (American Rhododendron Society 2015). Horticulturists and plant DANNY SCHISSLER enthusiasts commonly split the genus Rhododendron into two informal groups, “rhododendrons” and “azaleas,” based on appearance. Rhododendrons are typically considered to be large evergreen shrubs with large, leathery, elepidote (without scales) leaves, or smaller evergreen shrubs with lepidote (with scales) leaves. Rhodo- dendrons are also differentiated from aza- leas in flower morphology by the presence of 10 or more stamens (Azalea Society of America 2016). Azaleas, in contrast, are usually considered to be smaller, some- times deciduous shrubs with pubescent leaves and five to six stamens, though these morphological characteristics can be quite varied within species (Aza- lea Society of America 2016). The word azalea is derived from the Greek azaleos meaning “growing in dry soil.” This name reflected the cliffside and mountain habitats of Rhododendron luteum (yellow azalea), a European spe- cies (Lee et al. 1953). However, this is a misleading name because azaleas Azaleas typically have five stamens that are often strongly exserted, as are generally intolerant of drought and seen on this Alabama azalea (Rhododendron alabamense, 137-2005-E). are most commonly found in moist or Table 1: North American deciduous azaleas at the Arnold Arboretum

Representative Species Distribution Flowering Details Accession Blooms April-May. ​Rhododendron alabamense AL, FL, GA, MS, TN 137-2005 Mostly white flowers, some pink coloration.

AL, GA, KY, MD, MS, Blooms June-August. ​R. arborescens NC, NY, PA, SC, TN, 464-81 White, fragrant VA, WV

Blooms April-May; June in DE, GA, MD, NC, NJ, ​R. atlanticum 108-2007 northern gardens. White/ PA, SC, VA pink, very fragrant. Blooms March-April in wild, ​R. austrinum AL, FL, GA, MS 1403-85 later in northern gardens. Yellow/orange, fragrant.

AL, CT, GA, KY, MD, Blooms May-June. Variable ​R. calendulaceum MS, NC, NY, OH, PA, 109-2007 color, from pink/orange/red- SC, TN, VA, WV orange depending on source.

AL, AR, DE, FL, GA, Blooms March-April; ​R. canescens KY, LA, MD, MS, NC, 468-81 May in northern gardens. SC, TN, TX Pink/white.

​R. occidentale CA, OR 21743 (hybrid)

AL, CT, GA, IL, KY, MA, MD, NC, NH, Blooms April-May. R. periclymenoides 111-2007 NY, OH, PA, RI, SC, Varying shades of pink. VA, VT, WV

AL, AR, CT, GA, IL, KY, MA, MD, ME, ​R. prinophyllum MO, NC, NH, NY, 805-86 Blooms May. Pink. OH, OK, PA, RI, TX, VA, VT, WV

Late blooming, July- ​R. prunifolium AL, GA 815-90 September. Vivid orange/red.

Blooms April-May. ​R. vaseyi NC 1438-85 Varying shades of pink. Vulnerable in wild.

AL, AR, CT, DE, GA, LA, MA, MD, ME, May-August. White/pink, ​R. viscosum MO, MS, NC, NH, 112-2007 depending on germplasm NJ, NY, OK, PA, RI, source. Fragrant. SC, TX, VA, VT, WV

AZALEA SOCIETY OF AMERICA 2016 AL=Alabama, AR=Arkansas, CA=California, CT=Connecticut, DE=Delaware, FL=Florida, GA=Georgia, IL=Illinois, KY=Kentucky, LA=Louisiana, MA=Massachusetts, MD=Maryland, ME=Maine, MO=Missouri, MS=Mississippi, NC=North Carolina, NH=New Hamp- shire, NJ=New Jersey, NY=New York, OH=Ohio, OK=Oklahoma, OR=Oregon, PA=Pennsylvania, RI=Rhode Island, SC=South Carolina, TN=Tennessee, TX=Texas, VA=Virginia, VT=Vermont, WV=West Virginia 18 Arnoldia 74/2 • October 2016

mesic forest sites (Hume 1948). Considered a the assimilation of the North American decid- distinct genus (Azalea) until the mid-twenti- uous azaleas as a section within the broader eth century, azaleas were moved into the genus subgenus Hymenanthes, which includes many Rhododendron after Sleumer’s taxonomy was large-leafed evergreen Rhododendron species. published in 1949 (Chamberlain et al. 1996). Nonetheless, “azalea” and “rhododendron” Such taxonomies—the relationships of remain important horticultural terms for mar- species based on morphological traits and, keting and identification purposes. increasingly, genetic variation—are complex and frequently revised in a large genus like Rhododendron in the Garden Rhododendron as new species are discov- The earliest recorded cultivation of plants in ered. Traditional morphology-based taxonomy the genus Rhododendron began in the fifteenth uses leaf, bud, floral, and other physical traits century in Japan and involved a cultivar group to determine relationships between species. now known as the Satsuki azaleas, derived from However, this kind of physical classification the former Tsutsusi, or subgenus of evergreen can confuse convergent evolution (evolution azaleas (Callaham 2006). At the time, only of similar adaptations independently across the rich and privileged classes in Japan were varying taxa) with species similarity, leading allowed to grow and possess azaleas as they to incorrect conclusions about species relation- were deemed “too beautiful” for commoners ships. Modern molecular-based taxonomy uses (Callaham 2006). Early botanical explorers such differences in DNA sequence to group species as Robert Fortune in Asia and John Tradescant based on the likelihood of previously shared in colonial North America first brought Rho- ancestry. Since this is based on the timespan dodendron to prominence through their plant back to the most recent common ancestor, the collecting activities in the eighteenth and nine- classifications will not be confused by conver- teenth centuries (Cox et al. 1997). They dis- gent evolution of morphological traits. In the covered diverse flower color, leaf morphology, genus Rhododendron, subsequent molecular and plant habit across the Rhododendron spe- phylogenies that group species based on genetic cies they encountered. Soon after these plants variation have shown no distinction between appeared in European gardens, plantsmen species commonly known as azaleas and rhodo- began creating interspecific hybrids. The great dendrons (Goetsch et al. 2005). This has led to diversity in flower colors, fragrance, plant size, ALEXANDER Q. SUSKO ALEXANDER Q. SUSKO

Swamp azalea (Rhododendron viscosum) has a very wide native range and variable growth habit. Flowers are typically white, as seen on this tagged plant (left) growing near the Fourche la Fave River in the Ouachita National Forest near Y City, Arkansas, but pink flowers also occur, as on this plant (right) found in another population within the Ouachita National Forest, this one near Eagleton, Arkansas North American Deciduous Azaleas 19

The Ghent Hybrid Azaleas The Ghent hybrid azaleas resulted from crosses between the European native azalea R. luteum (yellow azalea) and a number of North KYLE PORT American species including R. calendulaceum (flame azalea), R. periclymenoides (pinxterbloom azalea), and R. viscosum (swamp azalea) (Dirr 1998). Initial crosses were made in Ghent, Belgium, start- ing around 1820, additional hybrid- ization occurred in England, and many Ghent hybrid cultivars were introduced, primarily from Belgium, in the following decades. Although the parentage is quite mixed, these hybrids are often grouped together under the name R. × gandavense. They are notable for their often fragrant flowers that come in a wide range of colors. The Ghent hybrids lost popularity as other hybrid aza- The brightly colored flowers of Ghent hybrid azalea cultivar ‘Reine des Rouges’ leas were introduced, but 22 Ghent (accession 623-61-A) show a resemblance to those of flame azalea (R. calendula- cultivars can still be seen in the ceum), one of the parent species originally used in hybridizing the Ghent azaleas. Arnold Arboretum collections.

leaf shape, and leaf pubescence (indumentum) and cold hardiness among deciduous azaleas resulting from these efforts led to expanded has long generated interest for using North horticultural interest in rhododendrons and American species in breeding. John Bannister, azaleas in the early twentieth century (Hume an English botanist, recorded the first decidu- 1948). Throughout the twentieth century, ous azalea in North America, Rhododendron hobbyists played a major role in the prolifera- viscosum (swamp azalea), in Virginia in 1690 tion of new cultivars (Galle 1974). Rhododen- (Galle 1974). Seeds from the newly discovered dron cultivation today spreads across temperate deciduous azalea species were sent back to regions of the world, and there are over 28,000 Europe where plants were grown for observa- named cultivars in existence (American Rhodo- tion beginning in 1734 by the American bota- dendron Society 2016). nist John Bartram. It was not until 1825 that the Deciduous azaleas in sect. Pentanthera are first recorded and popular interspecific hybrids represented by one species each in Europe, Asia, were produced using North American decidu- and western North America and 14 accepted ous azaleas (Hume 1953) (see textbox above). species in eastern North America (Towe 2004; Although they grow well within their native Zhou et al. 2008). Deciduous azaleas constitute ranges, lack of cold hardiness and/or intolerance the largest group of Rhododendron species in of high soil pH are major limiting factors to cul- North America. Because it holds such a large tivation of these azaleas across much of North number of species (compared to other parts of America. Relatively few Rhododendron species the world), the southeastern United States is are native to continental climates, typified by considered a major center of diversity for decid- extreme temperature variations throughout the uous azaleas (Hume 1953). The great amount of year and characteristic of many regions within phenotypic variation for flower color, fragrance, the United States. This is reflected in the culti- 20 Arnoldia 74/2 • October 2016 UNIVERSITY OF MINNESOTA

Research staff member Margaret Gearhart stands next to the original ‘Northern Lights’, a cold-hardy deciduous azalea cultivar, in June 1979 at the Minnesota Landscape Arboretum.

vation history of Rhododendron species, which, plasm (Hokanson 2010). For example, subur- until fairly recently, were only commonly banization in the United States following World grown and propagated in the mild and humid War II led to an increased need for landscaping climates of Japan, Europe, and the eastern and plants to beautify new developments (White- western coasts of North America. For woody hand and Larkham 1992). During the middle of plant breeders in the midwestern United States, the twentieth century, few ornamental plants developing cultivars for their tolerance to conti- adapted to the upper midwestern United States nental climates is of paramount importance for existed (UMN Fruit Breeding Farm 1954). Later, the horticultural success of deciduous azaleas. University Agricultural Experiment Stations in Fortunately, despite originating from milder states like Minnesota began funding breeding climates, individual genotypes from many programs for ornamental plants to develop and North American native azalea species have introduce promising cultivars for landscape use been identified that are exceptionally hardy (Widrlechner 1982). Many ornamental shrubs under extreme temperature variation (Widrlech- were trialed at the time on the grounds of the ner 1982). North American deciduous azalea newly founded Minnesota Landscape Arbore- germplasm has undergone relatively little tum, including several deciduous azalea species systematic evaluation and had received little and interspecific hybrids developed previously breeding focus until the twentieth century, in Europe. After years of parental and seed- when diversified landscape needs led nursery ling testing, plants from crosses made in 1957 growers to seek hardier Rhododendron germ- between mollis azaleas (R. × kosteranum), North American Deciduous Azaleas 21

which are a group of Asian hybrid deciduous other abiotic stresses in natural Rhododendron azaleas, and the American species R. prino- sect. Pentanthera populations remains limited. phyllum proved to be hardy to at least -35°C Tolerance to abiotic stressors such as winter (-31°F) (Johnson and Snyder 1966). One seedling cold, summer heat, soil pH, and soil salinity from this breeding population later became the are necessary for successful plant growth both cultivar ‘Northern Lights’ and was released in in natural and cultivated settings. Abiotic stress 1978 as part of the Northern Lights Series, the tolerance in woody species like deciduous first flowering azaleas bred for midwestern cli- azaleas can arise genetically through human- mates (Pellett and Vos 1978). The University of mediated or natural selection. However, a lack Minnesota woody landscape plant breeding of understanding about the nature of adaptive program has maintained the longest stand- genetic variation for such traits is not unique ing breeding program for deciduous azaleas to azaleas; a knowledge gap is common across in North America, and continues to actively woody plants and impedes understanding of release cultivars under the Northern Lights their maximum adaptation in both horticul- Series today (Widrlechner 1982; Hokanson 2010; tural and ecological contexts. Genetic variation, Hokanson et al. 2015). or variation in the DNA sequences between individuals in a species, is often a major factor Identifying Adaptive Genetic Variation in influencing the adaptation of an individual Though certain stress tolerances (cold hardiness to an environment. In situations when indi- in particular) of azaleas within the University viduals possessing certain patterns of genetic of Minnesota breeding program are well doc- variation reproduce more successfully under umented, understanding of trait variation for an environmental stress, genetic variation is NANCY ROSE

An azalea breeding trial bed at the University of Minnesota Horticultural Research Center includes introduced culti- vars ‘Lemon Lights’ (left) and ‘Northern Hi-Lights’ (foreground) as well as numbered selections. 22 Arnoldia 74/2 • October 2016 ALEXANDER Q. SUSKO

Open longleaf pine (Pinus palustris) forest is a typical habitat for Rhododendron viscosum subpopulations in the Apalachicola National Forest near Tallahassee, Florida.

considered to be adaptive. Adaptive genetic tion. It is imperative to understand such genetic variation and associated traits are inherited by variation in breeding populations if horticul- offspring; identifying such traits is an important tural breeders wish to sustain the development (but time consuming) part of breeding all plants. of new, adapted cultivars. The development of the Northern Lights Series New research technologies present oppor- is a prime example: it took 21 years from evalu- tunities to more efficiently identify adaptive ating initial parents, making crosses, and field genetic variation for abiotic stress tolerance testing the seedlings before a reliably cold hardy in populations of North American deciduous cultivar was introduced. This is largely due to azaleas with important implications for culti- the biological constraints of breeding woody var development. Linking genomic sequence perennial species, including long juvenile and environmental data, an emerging approach periods (time prior to sexual maturity of the known as landscape genomics, makes it pos- plant) that slow the breeding process. This also sible to identify genetic variation in plant complicates efforts to understand the genetics populations that depend on an environmental behind important traits, further hindering the factor (Rellstab et al. 2015). It is through this discovery of potentially adaptive genetic varia- framework that genetic variation is declared North American Deciduous Azaleas 23

as potentially adaptive. Although some Arboretum is currently being used to test these follow-up experiments are necessary to confirm landscape genomic approaches by obtaining the adaptive nature of this genetic variation environmental data from the origin points of discovered using this approach, this advance- the accessions and performing genetic sequenc- ment gives scientists and breeders a new way ing on those accessions. The goal is to identify to quickly screen diverse wild germplasm potentially adaptive DNA variation in North to identify populations that display unique American deciduous azaleas that could benefit adaptations to the environment. future breeding efforts by identifying promis- Collections at the Arnold Arboretum and our ing species or populations as parents for future program’s prior sampling of wild populations cultivar development. For example, patterns of swamp azalea constitute an ideal source of of genetic variation might be detected when plants to help answer these types of research looking at a set of individual azaleas originat- questions. Most importantly, plants in this col- ing from environments with varying degrees of lection are linked to detailed information about average winter minimum temperatures. If an their collection locations that allow for rela- association is detected between patterns in the tionships between genetic and environmental genetic variation and average winter minimum variation to be investigated. North American temperature, it is possible that the genetic vari- deciduous azalea germplasm at the Arnold ation confers an adaptive advantage in those ALEXANDER Q. SUSKO ALEXANDER Q. SUSKO

Rhododendron austrinum (orange azalea; accession 1403-85) is Rhododendron vaseyi (pinkshell azalea; accession 657-70) is native primarily to the Florida panhandle and adjacent regions rare in the wild, with only a few known populations, all in in Mississippi, Alabama, and Georgia. It bears fragrant yellow North Carolina. The Arnold Arboretum has a number of con- and orange flowers. servation accessions of this beautiful pink-flowered azalea. 24 Arnoldia 74/2 • October 2016 KYLE PORT

Rhododendron prunifolium (plumleaf azalea) is a late-season (July to September) bloomer, bearing flowers in shades of red and orange. The flowers of Arnold Arbo- retum accession 815-90-J, seen here, are an especially vibrant cherry red. WILLIAM (NED) FRIEDMAN

Rhododendron calendulaceum (flame azalea; accession 109-2007-J) is notable for its brightly colored flowers that range from yellow to orange to bright red. This species is native to the Appalachian Mountains ranging from New York to Georgia. North American Deciduous Azaleas 25 NANCY ROSE

The flowers of Rhododendron periclymenoides (pinxterbloom azalea; accession 3237-C) range from white to pink to purplish pink. It grows in mesic forests and wetlands from New Hampshire and Vermont to Alabama. 26 Arnoldia 74/2 • October 2016 KYLE PORT

Rhododendron atlanticum (coastal or dwarf azalea; accession 108-2007-A) is native to coastal regions in the Mid-Atlantic and Southeast. Its white to light pink flowers are sweetly fragrant. NANCY ROSE

Rhododendron prinophyllum (roseshell azalea) has a wide native range from Maine to Georgia and Texas. Its flowers may be light to deep pink. North American Deciduous Azaleas 27

azalea populations. While existing deciduous Hokanson, S. C., S. T. McNamara, N. Rose, K. Zuzek, and azalea germplasm has been well characterized H. Pellett. 2015. ‘UMNAZ 493’ and ‘UMNAZ 502’; Two new cold hardy deciduous azalea for cold hardiness within the University of Min- selections from the University of Minnesota. nesota breeding program, many other sources HortScience 50(9)S:053 (Abstr.). of tolerance to abiotic stressors (e.g., heat, tem- Hume, H. H. 1948. Azaleas: Kinds and Culture. New perature variability, drought) remain to be iden- York: The MacMillan Company. tified within this group of plants. Hume, H. H. 1953. Azaleas and Camellias (Revised). New Such variation is of great interest to breeders York: The MacMillan Company. seeking to improve stress tolerance through breeding. The approaches introduced above Johnson, A. G. and L. C. Snyder. 1966. Breeding azaleas for Minnesota. Quarterly Bulletin of the American could be extended in the future towards Rhododendron Society 20:163–165. informing conservation efforts that leverage Lee, F. P., F. O. Coe, B. Y. Morrison, M. Perkins, and the adaptive potential of populations. For the F. Weiss. 1953. The Azalea Handbook. existing deciduous germplasm at the Arnold Baltimore: Monumental Publishing Company. Arboretum, this research will characterize the Pellet, H. and F. Vos. 1978. Northern Lights. Minnesota collection for its adaptive potential to com- Agricultural Experiment Station, Miscellaneous mon environmental stressors. Such efforts Report #155. could greatly inform future collection and Rellstab, C., F. Gugerli, A. J. Eckert, A. M. Hancock, conservation efforts for these species should and R. Holderegger. 2015. A practical guide any generate breeding or conservation interest to environmental association analysis in in the future. Ultimately, we hope that this landscape genomics. Molecular Ecology 24(17): approach will further enable the cultivation of 4348–4370. these North American horticultural gems in as Towe, C. L. 2004. American Azaleas. Portland, Oregon: many landscapes as possible. Timber Press. United States National Plant Germplasm System (GRIN), Literature Cited https://npgsweb.ars-grin.gov/gringlobal. Last accessed June 2016. American Rhododendron Society. http://www. rhododendron.org/. Last accessed January 2016. University of Minnesota Fruit Breeding Farm. 1954. Report of the Fruit Breeding Farm Visitors Committee. Azalea Society of America. http://azaleas.org/. Last Minnesota Horticulturist, 82(9):143. accessed January 2016. Whitehand, J. W. R. and P. J. Larkham. 1992. Urban Callaham, R. Z. 2006. Satsuki Azaleas for Bonsai and Landscapes: International Perspectives. Hove, Azalea Enthusiasts. Passumpsic, Vermont: East Sussex, United Kingdom: Psychology Press. Stone Lantern Publishing. Widrlechner, M. 1982. Studies on the Breeding Chamberlain, D., R. Hyam, G. Argent, G. Fairweather, and Potential and Genetics of Hybrid Azalea, K. S. Walter. 1996. The genus Rhododendron: Rhododendron × Kosterianum Schneider × its classification and synonymy. Edinburgh, Rhododendron Prinophyllum (Small) Millias. Scotland: Royal Botanic Garden Edinburgh. St. Paul, Minnesota: University of Minnesota Cox, P. A. and K. N. Cox. 1997. The Encyclopedia of Doctoral Thesis. Rhododendron Species. Perth, Scotland: Zhou, W., T. Gibbons, L. Goetsch, B. Hall, T. Ranney, Glendoick Publishing. and R. Miller. 2008. Rhododendron colemanii: Dirr, M. A. 1998. Manual of Woody Landscape Plants A New Species of Deciduous Azalea (5th ed.). Champaign, Illinois: Stipes Publishing (Rhododendron section Pentanthera; Ericaceae) LLC. from the Coastal Plain of Alabama and Georgia. Journal American Rhododendron Society Galle, F. C. 1974. Azaleas. Birmingham, Alabama: 62(2): 72–78. Oxmoor House, Inc.. Goetsch, L., A. J. Eckert, B. D. Hall, and S. B. Hoot. 2005. Alexander Susko is currently a PhD student in the Applied The molecular systematics of Rhododendron Plant Sciences graduate program studying plant breeding (Ericaceae): a phylogeny based upon RPB2 gene and molecular genetics, James Bradeen is a professor and sequences. Systematic Botany 30:616–626. department head in the Department of Plant Pathology, Hokanson, S. C. 2010. “Lights” in the land of 10,000 lakes. and Stan Hokanson is a professor of woody plant breeding In: Rhododendrons, camellias and magnolias. and genetics in the Department of Horticultural Science, London: Royal Horticultural Society. all at the University of Minnesota, Twin Cities.