Reconsideration on the Origin of Cultivated Native to East Asia

Y. Teng K. Tanabe Department of Horticulture Faculty of Agriculture Zhejiang University Tottori University Hangzhou 310029 Tottori 689-5353 P.R. China Japan

Keywords: history of cultivation, natural distribution, nomenclature

Abstract The commercial native to East Asia are composed of five groups: Ussurian pear, Chinese white pear, Chinese sand pear, Xinjiang pear, and Japanese pear. It has been well known that Ussurian pear cultivars are derived from Pyrus ussuriensis, Chinese sand pear cultivars from P. pyrifolia grown wild in central and southern China. However, the origin of Chinese white pear cultivars and Japanese pear cultivars, and the genetic makeup of Xinjiang pears are still obscure. Chinese taxonomists have assigned cultivars of Chinese white pears to P. bretschneideri. Researchers outside of China speculated that P. bretschneideri might be a natural hybrid between P. betulifolia and cultivated P. pyrifolia, and Chinese white pear cultivars may originate from hybridisation between P. ussuriensis and P. pyrifolia. By means of RAPD analysis, we found RAPD markers specific to P. betulifolia or P. ussuriensis are not present in Chinese white pear cultivars. On the other hand, Chinese white pear cultivars are most closely related to Chinese sand pears based on analyses of RAPD markers, AFLP markers and SSR markers. A new nomenclature for Chinese white pear cultivars has been proposed: P. pyrifolia var. sinensis. As for the origin of native cultivars of Japanese pears, both our study and other researches using different DNA markers infer that at least some Japanese pear cultivars or their progenitors may have been introduced from ancient China and Korea. Xinjiang pears, mainly distributed in northwestern China, have been suspected to be of hybrid origin involving P. communis and Chinese white pears. However, RAPD analysis indicated that at least P. communis, P. armeniacifolia and Chinese white pears or sand pears have been involved in the origin of Xinjiang pears.

INTRODUCTION

Crop History of Pears in East Asia The pear is one of the most important fruit crops in temperate parts of the world. Pears have been cultivated for thousands of years in the world (Bell, 1991). In East Asia, China has a longest tradition of producing pears and the history of pear culture goes back at least 3000 years (Pu and Wang, 1963; Shen, 1980; Sun et al., 1983). Shi Jing, an ancient Chinese anthology of poetry (1000 BC), mentioned that “pears grow in wet low lands” (Shen, 1980; Sun et al., 1983). Dried pears have unearthed from the tumuli of more than 2000 years ago in Hunan Province and of 1500 years ago in Xinjiang Uygur Autonomous Region, China. The earliest record of pear culture dates back to before 720 in Japan (Kikuchi, 1948). According to ancient Chinese Literature, as early as 2000 years ago, pears had been grown in Korean peninsula (Lee and Hwang, 2002; Yoneyama, 2001). development has been continuous in China since early days. According to ancient Chinese literature, as early as 200 BC, Chinese people distinguished cultivated pears from wild species (Kikuchi, 1948; Shen, 1980; Sun et al., 1983). The earliest record of pear cultivars can be found in ancient Chinese book Shi Ji (100 BC). In Qi Min Yao Shu, an ancient agricultural science book written by Jia Sixie in 533-544, 17 cultivars have been recorded. Over long years of culture, different populations of pear cultivars have been developed to adapt to different environmental conditions. There are over 3000 local cultivars of pears distributed in China (Pu and Wang, 1963). Many of the pear cultivars originated hundreds of years ago are still widely cultivated in China. Until recently,

Proc. XXVI IHC – IVth Int. Symp. of Cultivated Ed. C.G. Davidson and P. Trehane Acta Hort. 634, ISHS 2004 175 Publication supported by Can. Int. Dev. Agency (CIDA) 200-300 years old pear trees were still grown commercially in some areas of China (Sun et al., 1983). In Shichuan village of Lanzhou City, Gansu Province, one ‘Dongguoli’ pear tree had a trunk circumference of 4.0 m and a height of 12 m and has been estimated to be 350 years old (Teng, unpublished data). In Japan, 200-300 years old pear trees are scattered from the North to the South (Yoneyama, 2001).

Taxonomy and Natural Distribution of Pear Species Native to East Asia Pears belong to the genus Pyrus. More than 900 infrageneric nomenclatures of Pyrus have been recorded (http://www.ipni.org), although only about 20 primary species are generally accepted by most taxonomists. According to their original distribution, pears can be arranged into two geographic groups: Occidental pears and Oriental pears (Bailey, 1917). Oriental pears distribute from Tian-Shan and Hindu Kush Mountains eastward to Japan, mainly in East Asia including China, Japan and Korea (Rubtsov, 1944). The modern botanical classification of native pears in East Asia began from the nomenclature of P. pashia Buch.-Ham. ex D. Don. in 1825. However, the taxonomy of pears native to East Asia was confusing and incomplete until 1915, when Rehder identified 12 species native to China. In 1937, the Chinese taxonomist R. Chen cited Rehder’s classification of pears in his book Taxonomy of the Trees in China. Thereafter, based on extensive investi- gation of pear germplasm throughout the country, Yu and Kuan (1963) described five new species. Presently, 13 pear species and a number of varieties are accepted by Chinese botanical taxonomists (Yu and Ku, 1974). It has been generally accepted that four species occur in Japan. In the Korean Peninsula, at least three species can be recognised. Native pear species in East Asia and their geographical distribution are listed in Table 1.

Cultivated Pears Native to East Asia Among Pyrus species, only a small number of species have been cultivated for commercial production. Of the Occidental pears, P. communis L. (the common pear) is the major cultivated species and has been widely produced throughout Europe, North and South America and Africa (Bell, 1991). The commercial pear cultivars native to East Asia are composed of five main groups: Ussurian pear (Qiuzili), Chinese white pear (Baili), Chinese sand pear (Shali), Xinjiang pear (Xinjiangli), and Japanese pear (Nashi). The former four types concentrate mainly in China and the last group has distribution in Japan. Besides the major cultivars, the minor cultivars originated from P. ×phaeocarpa Rehder and P. pashia are also grown in some areas of China (Pu and Wang, 1963; Yu, 1979). A few cultivars derived from Pyrus aromatica Kikuchi & Nakai occur in North Japan (Kikuchi, 1948). Traditional cultivars of P. communis are even found in Xinjiang and Gansu Provinces, China (Yuan and Du, 1980). It has been well known that Ussurian pear cultivars are derived from wild P. ussuriensis Maxim. The Ussurian pears are the coldest hardy of all pear cultivars and can endure -40°C to -50°C (Wang, 1996). The fruit of Ussurian pears are usually small globose and oblate with persistent calyx, and become soft and edible after a ripening period, which is clearly different from the crisp flesh texture of Chinese white pears, Chinese sand pears and Japanese pears (Table 2). The leaf morphology of Ussurian pears is also distinguished from that of other types of cultivars (Table 2). Chinese sand pears, P. pyrifolia (Burm. f.) Nakai, distribute in central and southern China, and bear fruit with smooth or russet skin. The shape, size and shelf life of fruit varies greatly with cultivars (Table 2). The wild P. pyrifolia occurs mainly in the Changjiang (Yangtze) River valley and still can be found in some areas of China. Chinese white pear cultivars are the most widely cultivated in China and occupy the most important position in commercial pear production. They grow further south than the Ussurian pears and their geographic distribution is just located between P. ussuriensis and P. pyrif oli a. Therefore, Rubtsov (1944) and Kikuchi (1946) proposed that the origin of Chinese white pears might be involved in hybridisation of P. ussuriensis and P. pyrifolia. Kikuchi (1946) put this group of cultivars under the name of P. ussuriensis var. sinensis Kikuchi. His nomenclature of Chinese white pears has greatly affected many

176 horticulturists in Japan. Many authors in Japan assigned cultivars of Chinese white pears to P. ussuriensis and one of the recent examples can be found in Okubo’s paper (2000). Because of the large difference in morphological characteristics, especially fruit traits between Ussurian pears and white pears (Table 2), Chinese taxonomists and horticulturists have never accepted this nomenclature. On the other hand, since Chen (1937) and Hu (1937) assigned Chinese white pear cultivars to P. ×bretschneideri Rehder, Chinese taxonomists and horticulturists have put Chinese white pear cultivars under the name of P. ×bretschneideri (e.g. Pu and Wang, 1963; Wang, 1996; Yu, 1979; Yu and Ku, 1974; Yuan and Du, 1980). Rehder (1915) named P. ×bretschneideri to refer those pears growing in North Hebei Province, which were suspected to be a hybrid between P. betulifolia Bunge and large-fruited cultivars (P. pyrifolia?) (Kikuchi, 1946). Kikuchi’s view about P. ×bretschneideri has been cited by other scholars such as Challice and Westwood (1973) and Bell (1991). Therefore, the relationship between Chinese white pear cultivars and P. ×bretschneideri is still to be solved. Japanese pears have been considered to be the same germplasm as Chinese sand pears and grouped into P. pyrifolia. The morphological characteristics of Japanese pear cultivars are similar to those of Chinese sand pears (Table 2). As for the origin of Japanese pear cultivars, the generally accepted opinion is that this group of cultivars have been domesticated from wild P. pyrif oli a, which was said to occur once in south Japan (Kikuchi, 1948). However, during his earlier lifetime, Kikuchi (1919) believed that no wild P. pyrifolia occurs in Japan. Until now, the community of wild P. p y r i f o l i a has never been found in any areas of Japan or recorded in the literature. So-called wild types were only found near human habitation and supposed to be escapes (Shimura, 1988). The progenitor of Japanese pear cultivars may have come from China and Korea (Shirai, 1929; Shimura, 1988). Xinjiang pear, P. ×sinkangensis Yu, has been suspected to be of hybrid origin involving P. c o m mu n i s and Chinese white pears based on their morphological characteristics (Yu and Kuan, 1963; Yu and Ku, 1974). According to Yu and Zhang (1979), cultivars of P. ×sinkangensis vary considerably, combining characteristics of both P. communis and Chinese white pears (Table 2). Generally, the fruit shape of this species is much similar to P. c o m mu n i s , but with a long pedicel. Some cultivars of P. ×sinkiangensis bear fruits with a persistent calyx and strong aroma, needing ripening before being edible, which is similar to P. communis. On the other hand, fruits of some cultivars are juicy and crisp and not needed for ripening, which is like Chinese white pear. Leaves of P. ×sinkiangensis are ovate, elliptic or broad ovate with fine serrate of the upper half margin and crenate or nearly entire of the lower half margin, and their sizes are intermediate between P. communis and Chinese white pears. Based on the facts mentioned above, the origin of Chinese white pear cultivars and Japanese pear cultivars is controversial, and the genetic makeup of Xinjiang pears is still obscure. Recently developed DNA markers, especially PCR-based markers have created the opportunity to solve these problems.

RECONSIDERATION ON THE ORIGIN OF CULTIVATED PEARS NATIVE TO EAST ASIA BASED ON DNA MARKERS There have been several DNA markers successfully used for identifying Asian pear cultivars and assessing genetic relationship of pears. New information has been obtained on the cultivated pears native to East Asia.

Chinese White Pears There is no evidence from our RAPD marker analysis (Teng et al., 2002) to support the two viewpoints on the origin of Chinese white pear cultivars: hybridization origin between P. ussuriensis and P. pyrifolia (Kikuchi, 1946; Rubtsov, 1944), and domestication origin from P. ×bretschneideri (Chen, 1937; Hu, 1937; Yu and Ku, 1974). We did not find any RAPD markers specific to P. betulifolia present in all 18 accessions of Chinese white pears, which infers that Chinese white pear cultivars most probably have no

177 relationships with P. ×bretschneideri. Except two cultivars native to North Hebei Province of China, which may be hybrids involving P. ussuriensis, all other Chinese white pear cultivars did not share species-specific RAPD markers with P. ussuriensis. When using Primer OPA-09, the unique band near 400 bp was observed for 18 Chinese cultivars of sand pears and white pears (42% of total). Moreover, in the dendrogram resulting from UPGMA based on RAPD data, Chinese white pear cultivars and Chinese sand pear cultivars clustered together into one group and some sand pear cultivars and white pear cultivars even further clustered into subgroup. All of these data indicate that Chinese white pear cultivars and sand pear cultivars share a common progenitor species, P. pyrifolia. Morphologically, Chinese white pear cultivars were much like Chinese sand pears (Table 2), which makes traditional taxonomy difficult. Taxonomists usually cannot distinctly classify the cultivars of Chinese pears with the smooth fruit skin, which are distributed in the transition belt between sand pears and white pears. A new name was proposed for Chinese white pear cultivars: P. pyrifolia var. sinensis Teng & Tanabe (Teng et al., 2002). Using simple sequence repeats (SSR) marker, Kimura et al. (2002) did not clearly separate Chinese sand pears and Chinese white pears from P. ussuriensis in a dendrogram. However, some Chinese white pear cultivars and sand pears cultivars were subclustered together.

Japanese Pear Cultivars In our study using RAPD marker, most Japanese pear cultivars fell into one main group in the dendrogram (Teng et al., 2002). One cultivar from Kyushu region and some cultivars from Kochi Prefecture were closely related to one Korean cultivar and some Chinese sand pear cultivars native to Zhejiang and Fujian Provinces and subclustered together. Furthermore, cultivars from Kochi Prefecture also showed high affinities to cultivars native to other regions. These results suggest that some local Japanese cultivars may have been derived from cultivars in Kochi Prefecture (also Kyushu Region?). Taking into consideration of flourishing trade and cultural exchanges through sea routes between Zhejiang Province and Kyushu Region/Kochi Prefecture during ancient period (Yoneyama, 2001), the progenitors of the latter may have been introduced from ancient China. Using restriction fragment length polymorphism (RFLP) of nuclear DNA, local cultivars native to Kochi Prefecture and regions along the Japan Sea were found to have some relationships with Chinese cultivars (Kawata et al., 1995). In order to confirm our inference, new accessions from Kochi Prefecture have been added and their genetic relationships with Chinese sand pear cultivars are being analyzed using RAPD and inter-simple sequence repeated (ISSR) markers. The preliminary results support our reference about Japanese pears (Fig. 1).

Xinjiang Pear Cultivars Xinjiang pears, P. ×sinkiangensis, usually produced complex RAPD profiles (Teng et al., 2001). Some RAPD markers in Xinjiang pear cultivars clearly come from Chinese sand pears or Chinese white pears and the other come from P. c o mmun is or P. armeniacifolia Yu. Artificial hybrids between Asian pear and P. co mmu nis closed indepen- dently with Xinjiang pear cultivars in the dendrogram based on RAPD data. Xinjiang pear cultivars native to Gansu and Qinghai Provinces are genetically distant with those native to Xinjiang. At least P. communis, P. armeniacifolia and Chinese white pears or sand pears have been involved in the origin of Xinjiang pears.

CONCLUSION New information from DNA-based markers indicates that the cultivars of Chinese sand pear, Chinese white pear and Japanese pear may have been originated from the common progenitor P. pyrifolia, which occurs in Central and South China. In our studies, only one local sand pear cultivar originated from Korea was included. In order to clarify genetic relationships among cultivars of P. pyrifolia native to East Asia, a further study will be needed using different DNA markers and large samples of local cultivars from

178 Korea, Kyushu Region of Japan, and Zhejiang and Fujian Provinces of China. Xinjiang pears have been suspected to be natural hybrids between Chinese white pears and P. communis. However, our study indicates that P. armeniacifolia has also been involved in the origin of Xinjiang pears.

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179 and Cultivars Native to East Asia Revealed by RAPD Markers. J. Amer. Soc. Hort. Sci. 127:262-270. Wang, Y. 1996. Chinese pears. China Agr. Sci. Press, Beijing. Yoneyama, K. 2001. Where do pears come from? Tottori ‘Nijisseiki’ Pear Museum, Kurayoshi City, Tottori Prefecture, Japan. Yu, T. 1979. Taxonomy of the fruit tree in China (in Chinese). China Agr. Press, Beijing. Yu, T. and Kuan, K. 1963. Taxa nova Rosacearum (1). Acta Phytotaxon. Sin. 8:202-236. Yu, T. and Ku, T. 1974. (1). Spiraeoideae-Maloideae. Flora Reipublicae Popularis Sinicae, vol. 36, Science Press, Beijing. Yu, T. and Zhang, P. 1979. Xinjiang pears, a new series of cultivars of pears in China. Acta Hort. Sin. 6:27-32. Yuan, F. and Du, S. 1980. Pears of northwestern China (in Chinese). Shaanxi Sci. and Technol. Press, Xian, People’s Republic of China.

Tables

Table 1. Pyrus species native to East Asia1).

Species Distribution 2n2) P. betulifolia Bunge North and Central China 34 P. calleryana Dcne. Central and South China, North Vietnam 34 P. dimorphophylla Makino Japan only P. fauriei C.K. Schneider Korea only P. koehnei C.K. Schneider South China, Taiwan P. xerophilla Yu Northwest China 34, 51 P. pashia Buch.-Ham. ex D. Don Southwest China, 34 P. pseudopashia Yu Southwest China 34 P. armeniacifolia Yu Xinjiang, China 51 P. ×phaeocarpa Rehder North China 34 P. ×hopeiensis Yu Hebei province, China 34 P. ×serrulata Rehder Hubei, Sichuan and Shannxi Province 34 P. taiwanese H. Iketani & Taiwan H. Ohashi P. ×sinkiangensis Yu Xinjiang Gansu and Qinhai Provinces 34 P. ×bretschneideri Rehder Hebei Province, China 34 P. ussuriensis Maxim. Northeast China, North Korea, Far East 34 Region of Russia P. pyrifolia (Burm. f.) Nakai (P. China, Japan and Korea 34 serotina Rehder) P. hondoensis Nakai & Kikuchi Japan Only P. aromatica Kikuchi & Nakai Japan Only 1) Adapted from Challice & Westwood (1973), Iketani and Ohashi (1993), Kikuchi (1948), Yu and Ku (1974). 2) The chromosome number is based on Pu et al. (1985). Besides P. armeniacifolia and some clones of P. xerophilla, some cultivars from P. pyrifolia, P. ×sinkiangensis and Chinese white pears were also identified to be polyploid.

180 Table 2. Main morphological characteristics of the cultivated pears native to East Asia1).

Chinese white pear Chinese sand pear Japanese pear Ussurian pear Xinjiang pear (Baili) (Shali) (Nashi) (Qiuzili) (Xinjianli) Leaf Shape Ovate, broad ovate Broad ovate Ovate Broad ovate to Ovate, elliptic or ovate broad ovate Base shape Broad cuneate, Broad cuneate, Broad cuneate, Subcordate, Ovate, obovate rotund, cordate rotund, cordate rotund rotund Size Large Large Large Large Medium to Large Margin Fine serrate-setose Fine serrate-setose Fine serrate-setose Coarse Upper half: Finely serrate-setose serrate; Lower half: crenate or nearly entire Fruit Size Medium to very Medium to very Medium to very Small to medium Medium to large large large large Skin Smooth Russet or smooth Russet or smooth Smooth Smooth smooth/ russet Shape Obovoid, ovoid, Oblate, globose, Oblate, globose, globose or oblate Ovoid to obovoid rarely globose obovoid obovoid, oblong Peduncle Generally long Short to long Short to long Short (1-2 cm) Long (4-5 cm) Calyx Deciduous Deciduous, Deciduous Persistent Persistent Carpel 5, rarely 4 5, rarely 4 5, rarely 4 5 5 Flesh Crisp & juicy Crisp & juicy Crisp & juicy Soft & Juicy Crisp & juicy or melting Shelf life Generally long Not so long as the Generally short, Short Short to long former a few long Ripening No No No Yes Yes/No 1) Characteristics of pears native to China are based on Pu and Wang (1963), Wang (1996) and Yu (1979); and to Japan are based on Kajiura and Suzuki (1980), Kikuchi (1948).

181 Figurese

Kochi1 Kochi2 Kochi6 Kochi27 Qiubaishali Chojuro Nijisseiki Kochi28 Kochi50 Kochi30 Imamuraaki Amanogawa Kochi29 Chosen Okoga Geishun Kochi11 Kawauchikoboku Ichiharawase Onba Shimoichikoboku Bingzili Mandingxueli Kochi24 Kuroki Kochi4 Kochi5 Kochi8 Kochi7 Kochi25 Kochi13 Kochi12 Shomeijinashi Kochi31 Shimokaburi Tsukutonashi Yiwulizi Umajiro Yoshinokobuku Tsukushiinunash Fukushima Tsugaruao Zongbaoli 1.00 4.25 7.50 10.75 14.00 Disimilarity coeficient

Fig. 1. Neighbor-joining tree for 43 pear accessions based on 306 RAPD markers and 64 ISSR markers. Cultivars native to China and Kochi prefecture were present in the most groups.

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