Abstract
Almonds and peaches are among the most economically important fruit crops in subtropical and temperate regions. Questions regarding the origin and domestication of the crop species, interspecific relationships, and evolutionary patterns of fruits have remained unanswered due to the lack of phylogenetic data of Prunus subgenus Amygdalus, in which both almond and peach are classified. Twenty-two species of subg. Amygdalus were included in phylogenetic analyses of plastid ndhF-rpl32, rpL16, trnH-psbA, trnL-trnF, trnQ-5′rps16, and trnS-trnG and nuclear s6pdh genes to investigate the circumscription of subg. Amygdalus, phylogenetic relationships among the species, and implication for mesocarp and endocarp evolution. Prunus subg. Amygdalus is best circumscribed to include both almonds and peaches, comprising two sections, Amygdalus and Persica. Species traditionally placed close to almonds, such as P. tenella, P. petunnikowii, P. triloba, and P. pedunculata, should be excluded from subg. Amygdalus. Characteristics used to diagnose subg. Amygdalus, such as dry, splitting mesocarp and the ornamentation of endocarp evolved multiple times in Prunus; thus classification based solely on these morphological characters produces a taxonomic scheme that might not represent common ancestry. A dry, splitting mesocarp is likely to be ancestral for the common ancestor of subg. Amygdalus, and the fleshy, non-splitting mesocarp found in peaches was derived from the dry, splitting mesocarp, presumably by domestication and selection for a fleshy fruit in China. Very low genetic divergence among cultivated almond and its close relatives might be associated with gene flow and/or rapid speciation within the group.
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References
Bentham G, Hooker JD (1865) Genera plantarum, vol 1. Lovell Reed & Co., London
Bortiri E, Oh S, Jiang J, Baggett S, Granger A, Weeks C, Buckingham M et al (2001) Phylogeny and systematics of Prunus (Rosaceae) as determined by sequence analysis of ITS and the chloroplast trnL-trnF spacer DNA. Syst Bot 26:797–807
Bortiri E, Oh S, Gao F, Potter D (2002) The phylogenetic utility of nucleotide sequences of sorbitol 6-phosphate dehydrogenase in Prunus (Rosaceae). Am J Bot 89:1697–1708
Bortiri E, Vanden Heuvel B, Potter D (2006) Phylogenetic analysis of morphology in Prunus reveals extensive homoplasy. Plant Syst Evol 259:53–71
Browicz K (1969) Amygdalus. In: Rechinger KH (ed) Flora Iranica, vol 66, Akademische Druck- und VerlagsansaltGraz, Austria, pp 166–187
Browicz K (1974) Distribution of woody Rosaceae in W. Asia: 13. Amygdalus webbii Spach and closely related species. Arbor Kornickie 19:5–21
Browicz K (1989) Conspect and chorology of the genera Amygdalus L. and Louiseania Carrière. Arbor Kornickie 34:31–54
Browicz K, Zohary D (1996) The genus Amygdalus L (Rosaceae): species relationships, distribution and evolution under domestication. Genet Resour Crop Evol 43:229–247
Carrière EA (1862) Amygdalopsis lindleyi. Revue Horticole. vol 1862. Librairie Agricole de la Maison Rustique, Paris, France, pp 91–93
Chin SW, Wen J, Johnson G, Potter D (2010) Merging Maddenia with the morphologically diverse Prunus (Rosaceae). Bot J Linn Soc 164:236–245
de Candolle AP (1825) Rosaceae. In: Prodromus systematis naturalis regni vegetabilis, vol 2. Treuttel & Würtz, Paris, France, pp 525–639
de Jussieu AL (1789) Genera plantarum. Herissant V, Paris, France
de Tournefort JP (1700) Institutiones rei herbariae, 1st edn. Paris, France
Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15
Edgar RC (2004) Muscle: multiple sequence alignment with high accuracy and high throughput. Nucleic Acid Res 32:1792–1797
Faust M, Timon B (1995) Origin and dissemination of peach. Horti Rev 17:331–379
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evol 39:783–791
Felsenstein J (1988) Phylogenies from molecular sequences: inference and reliability. Ann Rev Genet 22:521–565
Focke W (1888) Rosaceae. In: Engler A, Prantl K (eds) Die Natürlichen Pflanzenfamilien, vol 3, EngelmannLeipzig, Germany, pp 1–61
Goloboff P (1999) NONA (NO NAME) ver. 2. Published by the author, Tucumán, Argentina
Goloboff P, Farris S, Nixon K (2000) TNT (Tree Analysis Using New Technology). (BETA) ver. 1.1 Published by the authors, Tucumán, Argentina
Gradziel T (2011) Origin and dissemination of almond. Horti Rev 38:23–81
Gradziel T, Martinez-Gomez P, Dicenta F, Kester DE (2001) The utilization of related Prunus species for almond variety improvement. J Am Pomol Soc 55:100–108
Huelsenbeck JP, Ronquist F (2001) MrBayes: bayesian inference of phylogeny. Bioinformatics 17:754–755
Koehne E (1893) Prunus. Deutsche Dendrologie, 302–318. Verlag Von Ferdinand Enke, Stuttgart, Germany
Kovalev NV, Kostina KF (1935) A contribution to the study of the genus Prunus Focke (questions of taxonomy and plant breeding). Bull Appl Bot Genet Plant Br, ser. 8. Institute of Plant Industry, Leningrad, Russia, pp 1–76
Ladizinsky G (1999) On the origin of almond. Genet Resour Crop Evol 46:143–147
Lee S, Wen J (2001) A phylogenetic analysis of Prunus and the Amygdaloideae (Rosaceae) using ITS sequences of nuclear ribosomal DNA. Am J Bot 88:150–160
Lewis PP (2001) A likelihood approach to estimating phylogeny from discrete morphological character set. Syst Biol 50:913–925
Linnaeus C (1753) Species plantarum. Stockholm, Sweden
Lu LT, Bartholomew B (2003) Amygdalus. In: Flora of China, vol 9. Botanical Garden Press, St. Louis, USA
Mason SC (1913) The pubescent-fruited species of Prunus of the southwestern states. J Agri Res 1:147–177
Miller P (1754) The gardener’s dictionary, 4th edn. London, UK
Nixon KC (1999a) The parsimony ratchet, a new method for rapid parsimony analysis. Cladistics 15:407–414
Nixon KC (1999–2002) Winclada ver. 1.0000. Published by the author, Ithaca, New York, USA
Norup MV, Dransfield J, Chase MW, Barfod AS, Fernando ES, Baker WJ (2006) Homoplasious character combinations and generic delimitation: a case study from the Indo-Pacific arecoid palms (Arecaceae: Areceae). Am J Bot 93:1065–1080
Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817–818
Potter D, Gao F, Bortiri PE, Oh S, Baggett S (2002) Phylogenetic relationships in Rosaceae inferred from chloroplast matK and trnL-trnF nucleotide sequence data. Plant Syst Evol 231:77–89
Potter D, Eriksson T, Evans RC, Oh S, Smedmark J, Morgan DR et al (2007) Phylogeny and classification of Rosaceae. Plant Syst Evol 266:5–43
Rehder A (1940) A manual of cultivated trees and shrubs hardy in North America exclusive of the subtropical and warmer temperate regions, 2nd edn. Macmillan, New York
Roach FA (1985) Peaches and nectarines. In: Roach FA (ed) Cultivated fruits of Britain: their origin and history. Basil Blackwell Publisher Ltd, Oxford
Sambrook E, Fritzch F, Maniatis T (1989) Molecular cloning. Cold Spring Harbor Press, Cold Spring Harbor
Shaw J, Small RL (2004) Addressing the “hardest puzzle in American Pomology”: phylogeny of Prunus sect. Prunocerasus (Rosaceae) based on seven noncoding chloroplast DNA regions. Am J Bot 91:985–996
Shaw J, Lickey EB, Beck JT, Farmer SB, Liu W, Miller J, Siripun KC et al (2005) The tortoise and the hare II: relative utility of 21 noncoding chloroplast DNA sequences for phylogenetic analysis. Am J Bot 92:142–166
Shaw J, Lickey EB, Schilling EE, Small RL (2007) Comparison of the whole chloroplast genome sequences to choose noncoding regions for phylogenetic studies in angiosperms: the tortoise and the hare III. Am J Bot 94:275–288
Shimodaira H, Hasegawa M (1999) Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Mol Biol Evol 16:1114–1116
Simmons MP, Ochotorena H (2000) Gaps as characters in sequence-based phylogenetic analyses. Syst Biol 49:369–381
Simmons MP, Mueller K, Norton AP (2007) The relative performance of indel-coding methods in simulations. Molec Phylogenet Evol 44:724–740
Socias I, Company R (1998) Fruit tree genetics at a turning point: the almond example. Theor Appl Genet 96:588–601
Socias I, Company R, Felipe A (1987) Pollen tube growth and fruit set in a self-compatible almond selection. HortScience 22:113–116
Spach E (1843) Monographia generis Amygdalus. Ann Sci Nat Bot 19:106–128
Swofford DL (2002) PAUP*. Phylogenetic analysis using parsimony (* and other methods). Version 4.0b10. Sinauer Associates, Sunderland, Massachusetts, USA
Taberlet P, Gielly L, Pautou G, Bouvet J (1991) Universal primers for amplification of three non-coding regions of chloroplast DNA. Plant Mol Biol 17:1105–1109
Tavaré S (1986) Some probabilistic and statistical problems in the analysis of DNA sequences. In: Miura RM (ed) Some mathematical questions in biology—DNA sequence analysis. American Mathematical Society, USA, pp 57–86
Vander Wall S (2001) The evolutionary ecology of nut dispersal. Bot Rev 67:74–117
Wang YL (1985) Peach growing and germplasm in China. Acta Horti 174:51–55
Watkins R (1976) Cherry, plum, peach, apricot and almond. In: Simmons NW (ed) Evol Crop Plant. Longman, London, pp 242–247
Wen J, Berggren ST, Lee CH, Ickert-Bond S, Yi TS, Yoo KO, Xie L, Shaw J, Potter D (2008) Phylogenetic inferences in Prunus (Rosaceae) using chloroplast ndhF and nuclear ribosomal ITS sequences. J Syst Evol 46:322–332
Yang Z, Rannala B (1997) Bayesian phylogenetic inference using DNA sequences: a Markov Chain Monte Carlo method. Mole Biol Evol 14:717–724
Yazbek MM (2010) Systematics of Prunus subgenus Amygdalus: monograph and phylogeny. Ph.D. dissertation, Cornell University, Ithaca, New York, USA
Acknowledgments
The authors thank Ali Donmez for his help in providing collections from Turkey and Iran. They are grateful to Daniela Potter and an anonymous reviewer for their helpful comments. The first author thanks Jerold Davis, Maria A. Gandolfo, Kevin Nixon and Dennis Stevenson for their helpful comments. This work was supported by an NSF Doctoral Dissertation Improvement Grant (DEB-0709971) to Kevin Nixon and M.Y.
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Appendix 1: List of voucher specimens used in this study
Appendix 1: List of voucher specimens used in this study
DPRU accessions from the USDA National Clonal Germplasm Repository, Davis. An asterisk indicates that DNA was isolated from an herbarium specimen. Classification scheme follows Mason (1913) and Rehder (1940).
Prunus subg. Amygdalus
Sect. Amygdalus
P. arabica (Oliv.) Meikle var. arabica, Yazbek 23
P. arabica var. scoparia (1) Donmez 14114 (2) Donmez 14114b (3) DPRU 2224.1
P. argentea (Lam.) Rehder (1) Donmez 4379 (2) Donmez 12606 (3) Yazbek 09
P. balansae, Donmez 12609
P. bucharica (Korsh.) B. Fedtsch. ex Rehder, Al-Shehbaz & Hisoriev 601
P. carduchorum (Bornm.) Meikle, Donmez 10761
P. discolor S. K. Schneid., Donmez 4299
P. dulcis (Mill.) D. A. Webb. (1) Donmez 12603 (2) Donmez 12462 (3) Yazbek 05 (4) Yazbek 11
P. eburnea Aitch., DPRU 2226.8
P. erioclada Bornm. (1) Donmez 14161 (2) Donmez 14169
P. fenzliana Fritsch (1) Fayvush 509 (2) Al-Shehbaz & Hisoriev 654 (3) Donmez 5145
P. haussknechtii S. K. Schneid. (1) Donmez 14117 (2) Rechinger 47822*
P. kotschyi (Boiss. & Hohen. ex Spach) Meikle (1) Iranshahr & Terme 12677e* (2) Rechinger 49085*
P. kuramica (Korsh.) Kitam., DPRU 1467.4
P. lycioides (Spach.) S. K. Schneid. (1) Donmez 5085 (2) Donmez 14125
P. spinosissima (Bunge) Franch. (1) Donmez 14104 (2) Donmez 14104b (3) Donmez 14106 (4) Donmez 14125
P. trichamygdalus Hand.-Mazz., Donmez 12378
P. webbii (Spach) Fritsch (1) Donmez 3145 (2) Donmez 12164 (3) Donmez 12614
Sect. Persica
P. davidiana (Carrière) Franch. (1) DPRU 2325.3 (3) DPRU 2494.1 (3) Yazbek & Wang 15
P. kansuensis Rehder (1) DPRU 0582 (2) Yazbek & Wang 25
P. mira Koehne (1) DPRU 2232 (2) DPRU 2583.2 (3) Yazbek & Wang 50
P. mongolica Maxim. (1) Yazbek & Wang 01 (2) Yazbek & Wang 02
P. persica (L.) Batsch (1) DPRU 1586 (2) Yazbek 61 (3) DPRU 2595.1
P. tangutica (Bataline) Koehne (1) Yazbek & Wang 28 (2) Yazbek & Wang 30
Sect. Chamaeamygdalus
P. tenella Batsch (1) Barta 2005-237 (2) Barta 2005-239* (3) DPRU 2225.7 (4) Vitek s.n.
P. petunnikowii Rehder, no voucher
Prunus subg. Emplectocladus
P. eremophila Prigge, Donmez 10219
P. fasciculata (Torr.) A. Gray, Potter 752
Prunus subg. Prunus
Sect. Louiseania
P. triloba Lindley (1) Yazbek 65 (2) Yazbek & Wang 04
P. pedunculata (Pall.) Maxim., DPRU 2328.4
Sect. Penarmeniaca
P. fremontii S. Watson (1) DPRU 2097 (2) Potter 754
P. andersonii A. Gray, no voucher
P. havardii (W. Wight) S. C. Mason, Spelleberg et al. 9685
Sect. Armeniaca
P. armeniaca L., no voucher
P. mume (Siebold) Siebold & Zucc., Yazbek 49
P. sibirica L., Yazbek & Wang 56
Sect. Prunus
P. domestica L., no voucher
P. spinosa L., DPRU 0473
Sect. Piloprunus
P. texana Dietr., JSH924
P. maritima Marshall, JSH877
P. hortulana L. H. Bailey, JSH821-017
P. angustifolia Marsh., JSH785
P. nigra Aiton, JSH979
P. umbellata Elliott, JSH774
Outgroups
P. virginiana L., JSH871
Physocarpus amurensis (Maxim.) Maxim., JSH1015
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Yazbek, M., Oh, SH. Peaches and almonds: phylogeny of Prunus subg. Amygdalus (Rosaceae) based on DNA sequences and morphology. Plant Syst Evol 299, 1403–1418 (2013). https://doi.org/10.1007/s00606-013-0802-1
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DOI: https://doi.org/10.1007/s00606-013-0802-1