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Application of genomic technologies to crop plants: opportunities and challenges.

ENORMOUS GENOMIC RESOURCES have been developed for model plants such as Arabidopsis thaliana (L.) Heynh. and rice (Oryza sativa L.), including detailed genetic maps (Harushima et al., 1998), huge numbers of expressed sequence tags (ESTs) (Sasaki et al., 1994; Seki et al., 2002), deep-coverage large-insert [such as bacterial artificial chromosome (BAC)] libraries with extensive contig assemblies (Zhang et al., 1996; Mozo et al., 1998; Zhao et al., 2002), and both targeted and complete genome sequencing and annotation (Goff et al., 2002; Yu et al., 2002). These resources, coupled with the development of mutant stocks by knock-outs (Young et al., 2001) or targeted induced local lesions in genomes [TILLING (Till et al., 2003)], will allow for the efficient identification of gene(s) controlling phenotypes in model systems. However it is not clear how broadly applicable genetic associations revealed in model systems will be to economically important plants. Unquestionably, some genes identified in model plants will also condition economically important phenotypes in a crop plant. An example is the FLC locus that controls flowering in Arabidopsis (Michaels and Amasino, 1999) and in the closely related brassicas (Kole et al., 2001). Similar successes are readily communicated to the scientific community through publications; however, it will be difficult to publish, and therefore assess, the opposite scenario in which genes identified in model systems are not associated with similar traits in economically important plants. The purpose of this paper is to discuss some potential inconsistencies between model systems and economically important plants with onion (Allium cepa L.) as an example.

Recent studies have revealed that the Commelinanae and Asparagales are two strongly supported monophyletic sister groups within the monocots (Chase et al., 1995; Chase et al., 2000; Fay et al., 2000). The Commelinaloid monocots include the order Poales and possess the most economically important monocots, such as maize (Zea mays L.), rice, wheat (Triticum aestivum L.), etc. The Asparagales are the second most economically important monocot order and include important plants such as agave (Agave spp.), aloe (Aloe spp.), asparagus (Asparagus officinalis L.), chive (Allium schoenprasum L.), garlic (Allium sativurn L.), iris (Iris spp.), leek (Allium ampeloprasum L.), onion, orchid (Erycina spp.), and vanilla (Vanilla spp.). The "higher" Asparagales show successive microsporogensis, a cell plate is laid down after the first meiotic division, and form a well-defined group within the Asparagales (Fay et al., 2000). Economically important families in the "higher" Asparagales include the Alliaceae (chive, garlic, leek, and onion), Amaryllidaceae [various ornamentals and yucca (Yucca sp. L.)], and Asparagaceae (asparagus).

Genetic analyses of the Asparagales are hampered by longer generation times, severe inbreeding depression, and relative high cost of doing crosses. In addition, the nuclear genomes of the Asparagales are among the largest of all eukaryotes (Bennett and Smith, 1976; Ori et al., 1998). For example, onion has a nuclear genome of 16 415 megabasepairs per 1C, approximately equal to wheat and approximately 34 and 6 times larger than rice and maize, respectively (Arumuganathan and Earle, 1991). In contrast to wheat as a disomic hexaploid or maize as an ancient tetraploid (Celarier, 1956; Anderson, 1945), onion is a diploid (2n = 2x = 16) with no evidence of recent polyploidization contributing to its enormous nuclear genome. [C.sub.o]t reassociation kinetics demonstrated that the onion genome consists of middle-repetitive sequences occurring in short-period interspersions among single-copy regions (Stack and Comings, 1979). Biochemical and cytological analyses, as well as genetic mapping, indicated that intrachromosomal tandem duplications may have contributed to increased chromosome sizes in onion (Jones and Rees, 1968; Ranjekar et al., 1978; King et al., 1998). The extremely large nuclear genome of onion represents a huge challenge for the development of genomic resources. For example, a BAC library of onion with 99% probability of having any single copy region would require 503 957 clones of 150 kilobases. In comparison, similar coverage libraries of rice and maize would require 15 041 and 82 000 similarly sized clones, respectively. The development of genomic resources using species with smaller nuclear genomes will be imperative for the identification and cloning of economically important genes from onion.

Conservation of the linear order of genes (synteny) on chromosomes among related species is well documented for the Poaceae (Ahn et al., 1993; Dunford et al., 1995; Devos and Gale, 2000), Solanaceae (Bonierbale et al., 1988; Tanksley et al., 1992), and between Arabidopsis and the brassicas (Lagercrantz 1998, Parkin et al., 2002). Significant synteny among related species will allow for the alignment of major economically important qualitative or quantitative trait loci across specific chromosome regions in major crops (Paterson et al., 1995; Maughan et al., 1996). The identification of candidate genes, either as ESTs or open-reading frames (ORFs) on genomic contigs, will be revealed by fine mapping and comparison of flanking molecular markers to the annotated sequences of model plants. These associations should augment our chances of developing efficient marker-facilitated selection of major and minor genes, significantly reducing or eliminating recombination between the marker and the desired genes. This is especially important for the application of marker-facilitated selection to open-pollinated populations at or near linkage equilibrium. We recently demonstrated linkage equilibrium between tightly linked molecular markers and the Ms locus in open-pollinated populations of onion (Gokce and Havey, 2002). Because economically important populations of some crop plants have been open pollinated since antiquity, genomic regions showing linkage disequilibrium may be very short and require essentially cloning of genes to tag important traits for marker-facilitated selection.

Many candidate genes will be identified by knocking out specific genes by transposon insertions or TILLING in model plants such as Arabidopsis thaliana. These knock-outs may affect structural genes and not reveal variation at trans-acting factors that control the expression of major structural genes. Pleiotropy will complicate our ability to predict the relationships between specific candidate genes and phenotypes, as well as the manipulation of the candidate genes. Finally, we may be surprised by the true gene(s) controlling a specific phenotype. An example of an unexpected relationship is nuclear restoration of male fertility in cytoplasmic-male-sterile (CMS) maize. The Rf2 locus of maize synthesizes an aldehyde dehydrogenase that operates by an inconspicuous mechanism to restore male fertility in CMS maize (Liu et al., 2001). An onion cDNA highly homologous to the maize aldehyde dehydrogenase mapped independently of male-fertility restoration in CMS onion (Gokce et al., 2002), revealing that different genes may condition the same phenotype in different crop plants.

These challenges not withstanding, the genomic resources developed for model plants will reveal a plethora of candidate genes and provide great insights into gene expression. In some cases genes identified in model systems will condition economically important phenotypes in crop plants. However, it remains imperative that we identify, clone, and understand specific gene(s) conditioning economically important phenotypes in our major crops. In many cases, large genomic clones of specific crop plants will be imperative for the isolation of genomic regions, either up or down stream from the structural gene, interacting with important trans-acting factors controlling gene expression. Deep coverage genomic libraries and targeted sequencing will be required for the identification, cloning, and manipulation of specific genes affecting economically important phenotypes in major crop plants.


The author acknowledges the support of an IFAFS grant from CSREES USDA.


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Michael J. Havey *

USDA-ARS and Dep. of Horticulture, Univ. of Wisconsin-Madison, 1575 Linden Drive, Madison, WI 53706. Received 23 July 2003. * Corresponding author (
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Title Annotation:Symposium
Author:Havey, Michael J.
Publication:Crop Science
Geographic Code:1USA
Date:Nov 1, 2004
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