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From Forest to Field: Perennial Fruit Crop Domestication

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From Forest to Field: Perennial Fruit Crop Domestication American Journal of Botany 98(9): 1389–1414. 2011. SPECIAL PAPER F ROM FOREST TO FIELD: PERENNIAL FRUIT CROP DOMESTICATION 1 Allison J. Miller 2,4 and Briana L. Gross3 2 Department of Biology, Saint Louis University, 3507 Laclede Avenue, Saint Louis, Missouri 63103 USA; and 3 USDA-ARS, National Center for Genetic Resource Preservation, 1111 S. Mason Street, Fort Collins, Colorado 80521 USA • Premise of the study: Archaeological and genetic analyses of seed-propagated annual crops have greatly advanced our under- standing of plant domestication and evolution. Comparatively little is known about perennial plant domestication, a relevant topic for understanding how genes and genomes evolve in long-lived species, and how perennials respond to selection pres- sures operating on a relatively short time scale. Here, we focus on long-lived perennial crops (mainly trees and other woody plants) grown for their fruits. • Key results: We reviewed (1) the basic biology of long-lived perennials, setting the stage for perennial domestication by con- sidering how these species evolve in nature; (2) the suite of morphological features associated with perennial fruit crops under- going domestication; (3) the origins and evolution of domesticated perennials grown for their fruits; and (4) the genetic basis of domestication in perennial fruit crops. • Conclusions: Long-lived perennials have lengthy juvenile phases, extensive outcrossing, widespread hybridization, and limited population structure. Under domestication, these features, combined with clonal propagation, multiple origins, and ongoing crop – wild gene fl ow, contribute to mild domestication bottlenecks in perennial fruit crops. Morphological changes under do- mestication have many parallels to annual crops, but with key differences for mating system evolution and mode of reproduc- tion. Quantitative trait loci associated with domestication traits in perennials are mainly of minor effect and may not be stable across years. Future studies that take advantage of genomic approaches and consider demographic history will elucidate the genetics of agriculturally and ecologically important traits in perennial fruit crops and their wild relatives. Key words: artifi cial selection; clonal propagation; crop evolution; domestication; genetic bottleneck; perennial plants. For over 150 years, evolutionary biologists have used do- artifi cial selection causes cultivated populations to diverge mestication as a way to study selection under controlled condi- morphologically and genetically from their wild progenitors tions ( Darwin, 1859 , 1899 ; de Candolle, 1886 ); accordingly, ( Clement, 1999 ; Emshwiller, 2006 ; Pickersgill, 2007 ). The do- domesticated systems have occupied a critical role in the devel- mestication process produces a continuum of plant populations, opment and testing of evolutionary theory ( Ross-Ibarra et al., ranging from exploited wild plants to incipient domesticates to 2007 ; Pickersgill, 2009 ; Purugganan and Fuller, 2009 ). Recent cultivated populations that cannot survive without human inter- archaeological, genetic, and genomic analyses of annual crops, vention ( Clement, 1999 ; Pickersgill, 2007 ; Clement et al., such as maize ( Zea mays L.), rice ( Oryza sativa L.), sunfl ower 2010 ). Here, we consider cultivated plant species that are evolv- ( Helianthus annuus L.), tomato ( Solanum lycopersicum L.), ing in response to artifi cial selection pressures to be undergoing and wheat ( Triticum L. spp.), have greatly advanced our under- domestication. This inclusive approach requires that cultivated standing of plant domestication ( Doebley et al., 2006 ; Zeder populations exhibiting any morphological or genetic divergence et al., 2006 ; Bai and Lindhout, 2007 ; Burke et al., 2007 ; Burger from their wild ancestors be treated as part of the domestication et al., 2008 ; Gl é min and Bataillon, 2009 ). However, compara- continuum. tively little is known about the way in which perennial plants Perennial species include herbaceous plants as well as woody respond to artifi cial selection ( Zohary and Spiegel-Roy, 1975 ; shrubs and trees that live for more than 2 years. They are gener- Zohary, 2004 ; Clement et al., 2010 ; McKey et al., 2010 ), a rel- ally divided into two groups: short-lived perennials, which live evant topic for understanding how genes and genomes evolve for 3 – 5 years, and long-lived perennials, which live for more in long-lived species, and how perennial populations respond to than 5 years. In addition to living longer than annual plants, the other selection pressures operating on a relatively short time reproductive biology of perennials differs from that of annuals scale, such as contemporary climate change ( Hamrick, 2004 ; in that many perennials have long juvenile phases, are obligate Reusch and Wood, 2007 ). outcrossers, experience high rates of intra- and interspecifi c Plant domestication is an evolutionary process operating un- gene fl ow, and frequently reproduce both sexually and asexu- der the infl uence of human activities ( Harlan, 1992 ). Over time, ally ( Petit and Hampe, 2006 ; Savolainen et al., 2007 ; Smith and Donoghue, 2008 ; Vallejo-Mar í n et al., 2010 ). Under domesti- cation, perennial plants are often propagated clonally, which, in 1 Manuscript received 22 December 2010; revision accepted 31 May 2011. addition to long juvenile phases, further decreases the number The authors thank G. K. Croft, J. H. Knouft, D. M. Spooner, J. L. Strasburg, members of the Miller laboratory group, and two anonymous of sexual cycles separating domesticated individuals from their reviewers for valuable comments on previous versions of the manuscript. wild progenitors ( Zohary and Spiegel-Roy, 1975 ; McKey et al., 4 Author for correspondence (e-mail: [email protected]) 2010 , in press ). On the basis of life history characteristics and mode of reproduction, slow rates of evolution in perennial crops doi:10.3732/ajb.1000522 might be expected ( Zeder et al., 2006 ; Olsen and Schaal, 2007 ; American Journal of Botany 98(9): 1389–1414, 2011; http://www.amjbot.org/ © 2011 Botanical Society of America 1389 1390 American Journal of Botany [Vol. 98 Pickersgill, 2007 ); however, numerous perennial crops exhibit mestication by considering what is known about how trees substantial morphological and genetic divergence from their evolve under natural selection pressures, (2) defi ne the suite of wild progenitors. morphological features commonly associated with the evolu- Domesticated perennials are an important component of ag- tion of perennial fruit crops under domestication, (3) summa- ricultural economies around the globe ( Schreckenberg et al., rize present understanding of the origins and evolution of 2006 ). Perennial crops produce an abundance of useful prod- domesticated perennials grown for their fruits, and (4) describe ucts including fl eshy roots and other belowground materials the genetic basis of domestication in perennial fruit crops. (e.g., cassava, Manihot esculenta Crantz; horseradish, Armora- cia rusticana G. Gaertn., B. Mey. & Scherb.; potato, Solanum tuberosum L.; oca, Oxalis tuberosa Molina), woody stems [e.g., EVOLUTIONARY PROCESSES IN NATURAL Populus L. spp.; Douglas fi r Pseudotsuga menziesii (Mirb.) TREE POPULATIONS Franco], fl eshy fruits [e.g., apples, Malus × domestica Borkh.; avocados, Persea americana Mill.; sweet cherries, Prunus avium Although many important advances in evolutionary biology L.; oranges, Citrus sinensis (L.) Osbeck], and dry fruits [e.g., were made fi rst in crops and later tested in wild populations, it almonds, Prunus dulcis (Mill.) D. A. Webb; pecans, Carya il- appears that the opposite may be true for long-lived perennials, linoinensis (Wangenh.) K. Koch; walnuts, Juglans regia L.], where recent progress has occurred primarily in natural (undo- and interest in perennial grains is on the rise ( Glover et al., mesticated) tree populations. At neutral or nearly neutral genetic 2010 ). How perennial species respond to artifi cial selection de- loci (see Van Oosterhout et al., 2004 ), natural populations of pends in part on the lifespan of the individual (short-lived or long-lived species exhibit high levels of within population vari- long-lived perennial) and whether the target of selection is a ation and weak population structure ( Loveless and Hamrick, vegetative part of the plant (root, underground stem, above- 1984 ; Hamrick et al., 1992 ; Duminil et al., 2007 , 2009 ). Despite ground stem, leaf base, fl eshy leaf) or reproductive component this, these populations appear locally adapted, with multiple (fruit, seed). loci of small effect underlying adaptive traits ( Petit and Hampe, The majority of domesticated perennials are long-lived, woody 2006 ). Below, we provide a brief summary of recent evolutionary species cultivated for their edible fruits ( Van Tassel et al., analyses of natural tree populations and discuss their relevance 2010 ). Botanically, a fruit is a mature ovary; here, the term for understanding human-mediated evolutionary processes in “ fruit crops ” refers to cultivated plant species in which some long-lived species. component of the fruit is used by humans (e.g., mature ovary, On the basis of neutral marker data for natural populations, seed, additional fl ower parts attached to the mature ovary). limited population structure is correlated with lifespan: annu- Long-lived, perennial fruit crops were domesticated in all als are more structured than short-lived perennials, which are major agricultural centers
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