Chloroplast heterogeneity and historical admixture within the genus MalusAmerican Journal of Botany

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Authors
G. M. Volk, A. D. Henk, A. Baldo, G. Fazio, C. T. Chao, C. M. Richards
Year
2015
DOI
10.3732/ajb.1500095
Subject
Plant Science / Genetics / Ecology, Evolution, Behavior and Systematics

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A M E R I C A N J O U R N A L O F B OTA NY 102 ( 7 ): 1 – 11 , 2015 ; http://www.amjbot.org. This article is a U.S. Government work and is in the public domain in the USA.  © Botanical Society of America (outside the USA) 2015 • 1

A M E R I C A N J O U R N A L O F B O T A N Y

R E S E A R C H A R T I C L E

Apple trees cultivated for fruit production are primarily classifi ed as

Malus domestica , while ornamental crab apple trees originate from a number of wild and hybrid species. Malus domestica is an admixed species from a number of progenitor species, including M. sieversii ,

M. orientalis , M. sylvestris , and M. prunifolia ( Way et al., 1990 ;

Robinson et al., 2001 ; Luby, 2003 ; Velasco et al., 2010 ; Cornille et al., 2012 ; 2013 ). It is likely that apple has been domesticated many times throughout history. Malus domestica cultivars vary in their contributions from progenitor species ( Robinson et al., 2001 ;

Forte et al., 2002 ; Gross et al., 2012 ; Cornille et al., 2013 ; Nikiforova et al., 2013 ).

Th e primary center of origin for Malus is in Southwestern China ( Yunong, 1999 ), and this is still the most diverse region for wild

Malus . Malus species hybridize readily, and as a result, many Malus species have been described to explain the variable morphologies observed within this genus ( Luby, 2003 ). Traditionally, morphological traits have been used to diff erentiate Malus species ( Cuizhi and Spongberg, 2013 ). Due in part to the broad range of phenotypic variation, there has been a number of revisions and reclassifi cations within Malus ( Robertson et al., 1991 ; Robinson et al., 2001 ; Forte et al., 2002 ; Harris et al., 2002 ; Coart et al., 2006 ; Höfer et al., 2013 ).

Relatives of the domesticated apple, Malus domestica , are known to possess novel and desirable traits, such as biotic and abiotic stress resistance. For example, some individuals of M. sieversii and

M. orientalis exhibit resistance to apple scab, fi re blight, and cedar apple rust, and some individuals of M. prunifolia and M. sieversii are cold hardy and/or water-use effi cient ( Fischer and Fischer, 1999 ; 1 Manuscript received 9 March 2015; revision accepted 5 June 2015. 2 USDA-ARS National Center for Genetic Resources Preservation, 1111 South Mason

Street, Fort Collins, Colorado 80521; 3 USDA-ARS Dale Bumpers National Rice Research Center, 2890 Hwy. 130 E., Stuttgart,

Arkansas 72160; and 4 USDA-ARS Plant Genetic Resources Unit, 630 West North Street, Geneva, New York 14456-0462 5 Author for correspondence (Chris.Richards@colostate.edu) doi:10.3732/ajb.1500095

Chloroplast heterogeneity and historical admixture within the genus Malus 1

Gayle M. Volk 2 , Adam D. Henk 2 , Angela Baldo 3 , Gennaro Fazio 4 , C. Thomas Chao 4 , and Christopher M. Richards 2,5

PREMISE OF THE STUDY: The genus Malus represents a unique and complex evolutionary context in which to study domestication. Several Malus species have provided novel alleles and traits to the cultivars. The extent of admixture among wild Malus species has not been well described, due in part to limited sampling of individuals within a taxon.

METHODS: Four chloroplast regions (1681 bp total) were sequenced and aligned for 412 Malus individuals from 30 species. Phylogenetic relationships were reconstructed using maximum parsimony. The distribution of chloroplast haplotypes among species was examined using statistical parsimony, phylogenetic trees, and a median-joining network.

KEY RESULTS: Chloroplast haplotypes are shared among species within Malus . Three major haplotype-sharing networks were identifi ed. One includes species native to China, Western North America, as well as Malus domestica Borkh, and its four primary progenitor species: M. sieversii (Ledeb.) M. Roem.,

M. orientalis Uglitzk., M. sylvestris (L.) Mill., and M. prunifolia (Willd.) Borkh; another includes fi ve Chinese Malus species, and a third includes the three Malus species native to Eastern North America.

CONCLUSIONS: Chloroplast haplotypes found in M. domestica belong to a single, highly admixed network. Haplotypes shared between the domesticated apple and its progenitors may refl ect historical introgression or the retention of ancestral polymorphisms. Multiple individuals should be sampled within

Malus species to reveal haplotype heterogeneity, if complex maternal contributions to named species are to be recognized.

KEY WORDS apple; chloroplast sequence diversity; crop wild relatives; domestication; phylogenetic relationships; ploidy http://www.amjbot.org/cgi/doi/10.3732/ajb.1500095The latest version is at

AJB Advance Article published on July 14, 2015, as 10.3732/ajb.1500095.

Copyright 2015 by the Botanical Society of America 2 • A M E R I C A N J O U R N A L O F B O TA N Y

Zhi-Qin, 1999 ; Hokanson et al., 2001 ; Luby et al., 2001 , 2002 ; Volk et al., 2005 , 2008 ; Kumar et al., 2010 ; Bassett et al., 2011 ; Wan et al., 2011 ; LeRoux et al., 2012 ). A better understanding of the relationships between domesticated apple types and their wild progenitors will further breeding objectives for improvement ( Sestras et al., 2011 ;

Troggio et al., 2012 ).

In this work, we used chloroplast sequence data to estimate intraspecifi c heterogeneity, interspecifi c admixture, and phylogenetic relationships among 30 named Malus species represented in the

United States Department of Agriculture (USDA) Agricultural Research Service (ARS) National Plant Germplasm System (NPGS)— one of the world’s most comprehensive ex situ collections of Malus .

One objective of this research was to determine the geographic and phylogenetic distribution of Malus chloroplast haplotypes. In addition, we sought to describe the maternal lineages contributing to the domesticated apple.

MATERIALS AND METHODS

Plant materials— Th e USDA-ARS-NPGS apple collection in Geneva, New York, USA served as the source of leaves for DNA extractions. A total of 412 accessions representing 30 Malus species were included in these analyses (Appendix S1, see Supplemental Data with the online version of the article). Individuals were selected to represent all of the nonhybrid Malus species in the NPGS, with only one individual per seedling half-sibship. In addition, only one individual was selected from sets of identical genotypes, based on SSR data (particularly for M. hupehensis (Pamp.) Rehder apomicts and M. domestica ). Between 1 and 36 individuals represented each species. Th e nine individuals that are listed as M. pumila Mill. in the Genetic Resources Information Network (GRIN; U. S. Department of Agriculture, 2014 ) were designated as M. sieversii in our analyses, because of the high degree of similarity among the accessions associated with these two species names ( Volk et al., 2013 ; Kumar et al., 2014).