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Genomic Insights Into Date Palm Origins

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Genomic Insights Into Date Palm Origins G C A T T A C G G C A T genes Review Genomic Insights into Date Palm Origins Muriel Gros-Balthazard 1,* , Khaled Michel Hazzouri 2 and Jonathan Mark Flowers 1,3 1 Center for Genomics and Systems Biology, New York University Abu Dhabi, Saadiyat Island, P.O. Box 129188, Abu Dhabi, UAE; [email protected] 2 Khalifa Center for Genetic Engineering and Biotechnology (KCGEB), United Arab Emirates University, P.O. Box 15551, Al Ain, UAE; [email protected] 3 Department of Biology, Center for Genomics and Systems Biology, 12 Waverly Place, New York University, New York, NY 10003, USA * Correspondence: [email protected] Received: 16 September 2018; Accepted: 3 October 2018; Published: 17 October 2018 Abstract: With the development of next-generation sequencing technology, the amount of date palm (Phoenix dactylifera L.) genomic data has grown rapidly and yielded new insights into this species and its origins. Here, we review advances in understanding of the evolutionary history of the date palm, with a particular emphasis on what has been learned from the analysis of genomic data. We first record current genomic resources available for date palm including genome assemblies and resequencing data. We discuss new insights into its domestication and diversification history based on these improved genomic resources. We further report recent discoveries such as the existence of wild ancestral populations in remote locations of Oman and high differentiation between African and Middle Eastern populations. While genomic data are consistent with the view that domestication took place in the Gulf region, they suggest that the process was more complex involving multiple gene pools and possibly a secondary domestication. Many questions remain unanswered, especially regarding the genetic architecture of domestication and diversification. We provide a road map to future studies that will further clarify the domestication history of this iconic crop. Keywords: Phoenix dactylifera; domestication; next-generation sequencing; population genetics Highlights • A large amount of genomic data has been generated for the date palm in the past few years. • This review records these data and re-evaluates questions about date palm domestication origins and diffusion in light of genomic data • Remaining questions are highlighted, and the future perspective of the field discussed. 1. Introduction Plant domestication accompanying the development of agriculture is a significant step in human history. The understanding of the origins of crops is an important area of research involving scientists from many disciplines such as archaeology, anthropology, and, more recently, genetics and genomics. The main questions relate to where and when the plant was domesticated and what progenitor populations were involved. The molecular and phenotypic changes associated with domestication are also of prime interest. With the advent of next-generation sequencing (NGS) technologies, new advances have been made at an unprecedented pace. The availability of whole genome sequence data has indeed led to answers to many questions related to crop evolution. Such answers include a refinement of geographic origins (e.g., in African rice [1]) and the identification of genes controlling agronomically important traits (e.g., in maize [2]). This progress contributes to the awareness of human Genes 2018, 9, 502; doi:10.3390/genes9100502 www.mdpi.com/journal/genes Genes 2018, 9, 502 2 of 14 Genes 2018, 9, x FOR PEER REVIEW 2 of 14 awarenesshistory and of provides human history clues to and breeders provides who clues are developingto breeders tomorrow’swho are developing crops in thetomorrow’s context of crops global in thechange context [3,4 ].of global change [3,4]. The datedate palmpalm is is an an iconic iconic crop crop of hotof hot and and arid ar regionsid regions of North of North Africa Africa and the and Middle the East,Middle Figure East,1. FigureIt is a member 1. It ofis genusa memberPhoenix ofwhich genus consists Phoenix of 14 which perennial consists and dioecious of 14 monocotyledonousperennial and dioecious species monocotyledonousin the Arecaceae family species [5]. in the Arecaceae family [5]. FigureFigure 1. DistributionDistribution of of the the date date palm palm and Phoenix speciesspecies in Europe, Africa and Western Asia [[5,6].5,6]. The namesakenamesake fruitfruit of of the the date date palm palm can can be eatenbe ea freshten fresh or dried or dried or transformed or transformed into a largeinto a variety large varietyof products of products such as such syrup as or syrup paste. or The paste. sweet The fruit sweet has fruit played has a played prominent a prominent role in nomadic role in nomadic societies societiesof desert of regions desert and regions is firmly and is rooted firmly in rooted Arabic in culture. Arabic Eachculture. year, Each more year, than more eight than million eighttons million are producedtons are produced worldwide worldwide and this and number this isnumber constantly is constantly growing growing owing to owing large scaleto large efforts scale to efforts increase to increasethe numbers the numbers of fruit-producing of fruit-producing trees [7]. Thetrees date [7]. palm The isdate also palm a key is speciesalso a ofkey oasian species agrosystems of oasian agrosystemsas virtually every as virtually part of every the plant part finds of the a particularplant finds use a particular in daily life use [5 ]:in thedaily stipe life (or [5]: trunk) the stipe is used (or trunk)for construction, is used for theconstruction, leaves for the basketry, leaves andfor basket morery, importantly, and more importantly, the date palm the provides date palm a favorable provides amicroclimate favorable microclimate for the culture for of the other culture crops of in other an otherwise crops in an very otherwise harsh environment very harsh [environment8]. In cultivation, [8]. Inthis cultivation, species is reproducedthis species throughis reproduced a mixed through clonal-sexual a mixed system clonal-sexual although system clonal although propagation clonal is preferredpropagation in most is preferred circumstances in most to maintaincircumstances fruit quality to maintain [9]. Approximately fruit quality 3000[9]. Approximately cultivars are believed 3,000 cultivarsto exist [10 are], howeverbelieved thisto exist number [10], is however extremely this difficult number to assess.is extremely Indeed, difficult cultivars to areassess. supposedly Indeed, cultivarsclones bearing are supposedly the same clones name, bearing but cases the of same homonymy name, but have cases been of reportedhomonymy (e.g., have in been Morocco reported [11]) (e.g.,and, conversely,in Morocco individuals[11]) and, conversely, bearing the individuals same name bearing without the being same clonesname without have been being identified clones have (e.g., beenin Egypt identified [12]), making (e.g., in itEgypt difficult [12]), to making count and it difficult inventory to datecount palm and cultivars.inventory date palm cultivars. The history of domestication and diversificat diversificationion of the date palm has remained a puzzling question despitedespite decadesdecades ofof research research from from different differen disciplines.t disciplines. The The identity identity of itsof wildits wild progenitor progenitor has haslong long been been unknown unknown and hasand hampered has hampered research research into its into origins its origins [13]. The [13]. first The archaeological first archaeological records recordsof exploitation of exploitation and consumption and consumption of dates areof fromdates theare 6thfrom millennium the 6th millennium BCE [8]. There BCE is [8]. evidence There ofis evidencecultivation of incultivation the Gulf regionin the Gulf since region the late since 4th/early the late 3rd 4th/early millennium 3rd mill BCEennium while BCE seeming while to seeming appear tolater appear in Africa, later although in Africa, this shouldalthough be confirmedthis should by be further confirmed studies by [8]. further Many developmentsstudies [8]. Many in the developmentsunderstanding in of the the understanding date palm domestication of the date history palm domestication have been made history in the have past been decade made based in the on pastgenetics decade and based later genomics on genetics as the an genomed later genomics sequence becameas the genome available sequence and resequencing became available studies haveand resequencing studies have been carried out. In this paper, we review the genomic data available for Genes 2018, 9, 502 3 of 14 been carried out. In this paper, we review the genomic data available for the date palm and highlight the recent progresses made from this data on the question of origins. Further, we report the still remaining questions and propose a guideline to elucidate them. 2. High-Throughput Sequencing of Date Palms Next-generation sequencing refers to the numerous high-throughput alternatives to Sanger sequencing—the favorite sequencing method used since 1977—that were developed within the last decade and remain under active development [14]. These methods, and so-called 3rd generation technologies [15], enable the generation of genome assemblies (i.e., the haploid genome sequence of an organism) through de novo sequencing. Further resequencing studies allow the characterization of variation (e.g., single nucleotide polymorphisms (SNPs)) among individuals, populations, and species on a genome-wide scale. Although whole-genome resequencing is
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