RadishDB:Background

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Importance of radish as a crop and weed

Radish was already an important crop

In ancient Egypt over 5000 years ago, and was likely independently domesticated in China over 2000 years ago (Snow and Campbell 2005). The US radish crop was worth $50 million in 2000 (www.ers.usda.gov/briefing/Vegetables), and radish is certainly far more important in Asia, where a large variety of radishes are grown for their edible roots (including daikon) and others for edible leaves as fodder or for human consumption of seedpods (rat-tail radish; Snow and Campbell 2005).

Wild radish is a major pest of cereals and other crops worldwide

Especially winter wheat, and is a serious weed in at least 17 countries (Holm et al. 1997). It is the most damaging weed in small grains in the southwestern US (Schroeder 1989; Warwick and Francis 2005), where it can reduce winter wheat and canola yields by up to 80% as well as contaminate seed stock (Blackshaw et al. 2002; reviewed in Warwick and Francis 2005; www.ag.ndsu.nodak.edu/aginfo/entomology/ndpiap/Canola_GS/23weeds.htm). On Prince Edward Island, an average intensity wild radish infestation can cost potato farmers over [http:/www.organicagcentre.ca/Docs/OACC_Bulletin2_weeds_cost.pdf $3000 Cdn/hectare in reduced yield]. Radish is becoming a more serious pest, especially in the US and Australia, for at least two reasons. First, wild radish has evolved resistance to a variety of herbicides in Australia and South Africa (www.weedscience.org). Second, the increasing use of low-tillage practices to reduce soil erosion in the US makes wild radish harder to control (Culpepper et al. 2005). In addition, radish may become an even more serious agricultural weed in the future through hybridization with crop radish (see below). On the other hand, wild radish is increasingly used as a “green manure” to help control other weeds through the allellopathic chemicals produced by radish (Norsworthy 2003; Norsworthy and Meehan 2005).

The annual weed and crop radish have evolved from winter annual ancestors

Recent work in Conner’s lab on native European populations of R. raphanistrum show that these populations are winter annuals, forming a tight rosette with many leaves and bolting and flowering only after a cold treatment. This is in contrast to the populations of weedy radish that have been studied to date in a number of labs, which form little or no rosette and bolt and flower quickly. The crop radish also does not form a rosette and often flowers quickly; delayed flowering is a major goal for radish breeders (Curtis 2003; Snow and Campbell 2005). Thus, a major shift has occurred in the life history of radish under domestication and in becoming a serious worldwide weed. A molecular genetic understanding of this shift would provide fundamental insights into crop domestication, weed evolution, and life-history evolution in plants in general. Finding the gene loci responsible for this shift in radish will be greatly facilitated by the wealth of knowledge of the genetics of flowering in its relative A. thaliana, including many candidate genes such as CO, FT, FLC, FRI and GI (Simpson and Dean 2002); GI has been used to produce a later-flowering crop radish (Curtis 2003). Note that Arabidopsis also has annual and winter annual genotypes. To our knowledge, Brassica rapa is the only other serious weed species currently being sequenced, and Brassica and Raphanus each have the added advantage of containing both major crops and major weeds.

Wild radish is an invasive species of wild habitats in California (www.cal-ipc.org)

Norman Ellstrand’s group at UC Riverside has studied radish ecology and evolution for over 20 years (see below). They have found that the currently invasive radish in California is actually a hybrid between crop (R. sativus) and weedy (R. raphanistrum) radish, and that it has caused the extinction of both progenitor species in the wild. The invasive populations share a specific combination of traits from the crop and weedy ancestors, and the invasive is transgressive for one fitness-related trait – fruit weight is far greater in the hybrids than in either parent (Hegde et al. 2006). Ellstrand (pers. comm.) would use the markers developed by our proposed work and subsequent radish genetic map to find the genes and chromosome segments from each of the two parental species that affect the invasiveness of wild radish in California.

Model for assessing the transgene insertion and escape in crops

Radish was one of the first species for which crop to weed gene flow and subsequent hybrid fitness was measured (Klinger et al. 1991; Klinger and Ellstrand 1994). Allison Snow (Ohio State University) has established 15 replicate populations of experimentally-produced crop-wild radish hybrids in northern lower Michigan, and plans to submit an NSF LTREB proposal to expand this work to other locations (A. Snow, pers. comm.). The crop/weed hybrids had lower F1 fitness, but crop genes persisted over three years in the field (Snow et al. 2001). Snow (pers. comm.) would use the markers developed from the proposed sequencing to determine the specific genes and chromosomal segments from the crop that are retained in the hybrid weedy populations.

Radish as a model system in ecology and evolution

Below we give some examples of the diversity of ecological and evolutionary work on radish. The underlying themes of all of this research are adaptation to the biotic and abiotic environments (both natural and human-impacted) and some of the key traits involved in this adaptation; the breadth and depth of this work demonstrates that radish is one of the few true model systems in ecology and evolutionary biology. The cDNA sequence information we propose to produce will allow these studies to leap forward into the genomic era.

Plant-Insect interactions

The interactions between angiosperms and insects are key determinants of ecosystem structure and function, due to the dominance of these two groups in terms of numbers, biomass, and diversity. Herbivory is the main antagonistic plant-insect interaction, and pollination the main mutualism. Both have been extremely well-studied in wild radish.

Herbivory has a major impact on plant fitness, and is a major challenge for agriculture

Herbivory decreases female fitness (seed production) in radish. This decrease in fitness is known to occur both in response to chewing insects like caterpillars (Lehtila and Strauss 1999) and sucking insects like aphids (Snow and Stanton 1988), and the spatial and temporal patterns of leaf damage within a plant affect the magnitude of this decline (Mauricio et al. 1993).

Radish has evolved multiple induced defenses against this herbivory; the fitness costs, benefits, and quantitative genetics of these plastic responses to herbivory are well-known. Induced responses to herbivory are an important type of adaptive phenotypic plasticity, in which plants produce more defensive chemicals or structures after damage by herbivores. Feeding by herbivores on radish increases the density of defensive hairs (trichomes) on the leaves as well as toxic chemicals (glucosinolates) in the leaves, and these increased defenses reduce subsequent herbivory by both chewing and sucking herbivores and increased plant fitness relative to non-induced control plants (Agrawal 1998; Agrawal 1999; Agrawal et al. 2002). However, the induced defense has a cost, as the fitness of induced plants is decreased in the absence of later attack by herbivores (Agrawal et al. 1999b). The induced resistance was even transmitted to offspring through a maternal effect (Agrawal 2001; Agrawal et al. 1999a). The level of glucosinolate induction is heritable, demonstrating that continued selection for induction will result in continued evolution of this trait (Agrawal et al. 2002). The genomic tools enabled by the proposed cDNA sequencing would allow this work on induced defenses in radish to be taken to the molecular level. For example, the mechanisms of the inducible defenses could be uncovered by examining differences in gene expression between plants damaged by herbivores and others protected from damage. This is similar to work that an NSF Minority Postdoctoral Fellow in Conner’s lab, Gabriela Bidart-Bouzat, is undertaking in Arabidopsis, and is being done on model systems (Arabidopsis and tobacco) in other labs (e.g., Reymond et al. 2004; Voelckel and Baldwin 2003). A genetic map would be another approach toward finding the genes underlying resistance to herbivory; this approach has been used in Arabidopsis (Kliebenstein et al. 2001).

Pollination is a key mutualism for angiosperms, and is crucial for reproduction in crops, weeds, and native plants

Most studies of plant-pollinator interactions have been on plants that are specialized, that is, have only one or a few closely-related pollinator species, but many, perhaps most, plants are more generalized in their pollination. Radish is perhaps the best-studied of these generalist pollination systems. Radish has floral color polymorphisms, and different taxa of pollinators have different color preferences (Kay 1976; Kay 1978; Kay 1982; Stanton 1987). The different pollinator taxa also vary in their preference for floral size and number, and in their efficiency in removing and depositing pollen (Conner et al. 1995; Conner and Rush 1996). Conner’s lab would use a radish genetic map to find the genes affecting pollinator attraction and efficiency in radish, an intraspecific analogue to the work by Schemske and Bradshaw on crosses between two species of Mimulus (Bradshaw et al. 1998; Bradshaw et al. 1995; Bradshaw and Schemske 2003; Schemske and Bradshaw 1999).

Mechanisms of adaptation

The rate of adaptation of a complex (quantitative) phenotypic trait is determined by the product of the strength of natural selection, often quantified as the selection gradient (), and the G matrix comprising the additive genetic variances and covariances among the traits. The latter are often expressed in their standardized versions, heritability and genetic correlations. We have extraordinarily broad and deep knowledge of the strength of natural selection and the G-matrix for floral and life-history traits in wild radish, perhaps more so than for any other plant species.

Natural selection

Seed size is an important determinant of success in native as well as weedy and invasive plants; the causes and fitness consequences of seed size have been well-studied in radish. Maureen Stanton (UC Davis) has shown that there are both developmental and genetic components to seed size variation (Nakamura and Stanton 1989; Stanton 1984a), and that the developmental processes led to six-fold variation in seed size within single radish fruits. This within-fruit variation has strong fitness consequences in the field, as larger seeds were more likely to sprout, grew faster, and made more flowers than smaller seeds from the same fruit (Stanton 1984b). These differences resulted in differences in lifetime female fitness (Stanton 1985), a key evolutionary parameter. Selection through differences in male fitness (seed-siring success) is a crucial component of adaptive evolution in plants, but has been well studied only in radish. Half of all nuclear genes transmitted across generations are through pollen or sperm, that is, male function, but the vast majority of ecological and evolutionary studies of selection and fitness in plants measure only female fitness (numbers of seeds produced). Actual male fitness, estimated as the number of seeds sired using genetic marker-based paternity analysis, has been measured in wild radish more often than any other plant; indeed wild radish was one of the first plants in which this was done (Devlin et al. 1992; Devlin and Ellstrand 1990; Stanton et al. 1986). As a result, we know more about how herbivory and pollination affect lifetime male and female fitness, and more about selection on floral traits through male and female fitness in wild radish than we do for any other plant. For example, the work of Stanton’s group and Conner’s group show that selection on floral color (Stanton et al. 1986; Stanton et al. 1989) and floral morphology (Conner et al. 2003b; Conner et al. 1996a; Conner et al. 1996b; Morgan and Conner 2001; Stanton et al. 1991) is often stronger through male fitness than through female fitness. Strauss and Conner’s labs have shown that leaf damage by herbivores can affect attractiveness of the plant to pollinators and resulting male fitness (Lehtila and Strauss 1999; Strauss et al. 2001; Strauss et al. 1996). A key component of male fitness is pollen competition; we know more about pollen competition and its fitness effects in radish than perhaps any other plant. Diane Marshall of the University of New Mexico has been examining the processes that govern the success of pollen from different males deposited on the same flower for twenty years. She has found that multiple paternity within single wild radish fruits is common, and the relative success of pollen from different males is nonrandom, consistent across maternal plants, and occurs at least in part through interference competition (Ellstrand and Marshall 1986; Marshall 1988; Marshall 1998; Marshall et al. 2000; Marshall and Diggle 2001; Marshall and Ellstrand 1985; Marshall and Ellstrand 1986; Marshall and Ellstrand 1988; Marshall and Ellstrand 1989; Marshall and Folsom 1992; Marshall et al. 1996; Marshall and Fuller 1994; Marshall and Oliveras 2001). Work by other groups has shown that pollen competitive ability is both heritable (Snow and Mazer 1988) and strongly affected by the environment (Young and Stanton 1990), and that the deposition of pollen from multiple donors on a flower affects both maternal and offspring fitness (Karron and Marshall 1990; Karron and Marshall 1993; Marshall and Whittaker 1989; Snow 1990). Marshall would use genomic tools to measure gene expression in the pollen and stigmas in response to different pollination treatments (D. Marshall, pers. comm.).

Genetic variance and covariance (G-matrix)

Heritability and genetic correlations are known for a wide variety of radish traits (Conner and Via 1993; Mazer 1987a; Mazer 1987b; Mazer 1989; Mazer 1992, and the expression of additive genetic variance in radish is strongly affected by the environment (Conner et al. 2003a; Mazer and Schick 1991a; Mazer and Schick 1991b; Mazer and Wolfe 1992; Williams and Conner 2001; Young et al. 1994). However, we know little about the molecular genetic basis for these complex traits; Conner’s lab would use a genetic map and microarrays to gain a mechanistic understanding of the G matrix and changes in gene expression. Genetic correlations do not cause the expected evolutionary constraint in wild radish. Constraints on adaptive evolution have been of major interest since Gould and Lewontin (1979). Genetic correlations among traits have often been invoked as a cause of constraint (e.g., Arnold 1992; Clark 1987; Maynard Smith et al. 1985). The genetic correlation between the filament and corolla tube in R. raphanistrum flowers is one of the highest ever reported in nature (Conner and Via 1993), is caused by pleiotropy (Conner 2002), and is stable across environments, populations, and related species (Conner et al, submitted). Thus, this correlation should cause an evolutionary constraint, that is, a slowing of the evolution of the most adaptive combination of traits. However, contrary to this prediction, artificial selection produced rapid independent evolution of these traits, with little evidence for a constraint (Conner et al, submitted). Stanton and Young (1994) reported very similar results for petal size and pollen number in R. sativus. We already have extraordinarily broad and deep of knowledge about wild radish floral evolution including pollinator-mediated selection based on lifetime male and female fitness measured in six field seasons at two field sites, multiple quantitative genetic analyses conducted in both the field and greenhouse, and phylogenetic comparative studies across the family Brassicaceae. Therefore, the logical next step is an understanding of the molecular genetics of these traits, but this will be difficult without more comprehensive sequence data. To facilitate future QTL (linkage) and association (linkage disequilibrium) mapping, a dense molecular map is required. An EST sequencing project using cDNA from multiple samples would provide the infrastructure for developing resources such as an expression microarray and a linkage map.

Adaptation to global change

Radish has been used as a model system to study the potential for adaptation to a variety of anthropogenic global changes, from genetic variation for response to increased CO2 (Case et al. 1998; Curtis et al. 1996; Curtis et al. 1994) and frost tolerance (Agrawal et al. 2004), to phenotypic plasticity caused by increased UV-B radiation (Tevini et al. 1983) and air pollution (Kostkarick and Manning 1993). Genomic tools would allow a truly predictive approach to plant response to global change.

Importance of radish for comparative genomics

Sequencing efforts in related speices

In the family Brassicaceae, Arabidopsis thaliana has been fully sequenced, and sequencing projects are underway for A. lyrata as well as the very closely related Capsella rubella by the Joint Genome Institute. Sequencing projects are also underway for Brassica rapa and B. oleracea (Ayele et al. 2005; Yang et al. 2005), which are very close to Raphanus (see Overview above). Having sequence data available for Raphanus would provide the comparative genomics community with the ability to make hierarchical comparisons between replicate pairs of closely related genera that are more distantly related to each other, but still close enough for comparisons across the two pairs. Sequences from species pairs can be used to determine if genome-wide trends are consistent across related lineages; the data for these kinds of analyses are not currently available in plants. Specifically, the availability of Raphanus sequence will (a) improve gene annotation and facilitate the identification of novel coding and RNA genes, (b) allow the detection of positive and lineage-specific selection on plant genes, and (c) provide crucial details on gene gain and loss patterns in plant gene families.

Gene discovery and annotation through sequence conservation

The availability of multiple genomes facilitates gene prediction, because evolutionary conservation can be used to identify likely functional regions (Brent and Guigo 2004). For coding genes, dual genome (e.g. TWINSCAN, Korf et al. 2001) and multiple genome (e.g. phylo-HMM, Siepel and Haussler 2004) gene finders have been developed that significantly out-perform prediction programs that use a single genome. Thus, the proposed project will greatly facilitate dicot gene prediction using dual or multiple genome gene finders. In addition to protein coding genes, substantial RNA genes are likely present in the unannotated regions of eukaryote genomes (Meyers et al. 2006). Recent whole genome tiling array studies have revealed candidate expression signals in intergenic regions in humans (e.g. Kapranov et al. 2002; Bertone et al. 2004), Arabidopsis (Yamada et al. 2003; Stolc et al. 2005), rice (Li et al. 2006), and Drosophila (Stolc et al. 2004). The proposed project will generate cDNA information useful for identifying novel RNA genes and assist in the validation of putative RNA genes found in other organisms, especially plants.

Nature of selection on plant gene sequences

Comparisons of DNA polymorphism within species to divergence between species allows the identification of positively selected genes as well as the differentiation of weak from strong purifying selection (Hudson et al. 1987; McDonald and Kreitman 1991; Sawyer and Hartl 1992). In species such as Drosophila melanogaster, several studies have shown that substantial number of protein coding genes experienced positive selection (Fay et al. 2002; Sawyer et al. 2003). In humans, 9% of loci analyzed show rapid amino acid evolution (Bustamante et al. 2005). On the other hand, studies of Arabidopsis thaliana populations show that most substitutions are deleterious (Bustamante et al. 2002). The differences between Drosophila and Arabidopsis have been attributed to the primarily selfing Arabidopsis mating system (Bustamante et al. 2002). Therefore, to see if plant genes experience positive selection like other species, sequences from natural populations of outbreeding species like radish will be necessary. The proposed project will generate cDNA sequences both within and between radish species that will facilitate the identification of positive selection on plant genes. The availability of sequences from multiple species will also allow the identification of genes experiencing positive selection in the lineage-specific fashion (Clark et al. 2003); these are candidate genes for adaptive traits in radish.

Polyploidy, gene loss and retention

Polyploidy has occurred extensively in angiosperms and is recognized as a key factor in the evolution of plants and their genomes (Wendel 2000). Gene loss occurs frequently in polyploids; for example, more than 80% of genes were lost after the most recent polyploidization event in the Arabidopsis lineage (Blanc and Wolfe 2004). The high gene loss rate is corroborated by a sequence analysis of a 2.2 Mb region representing triplicated genome segments of Brassica oleracea, which are each paralogous with one another and homologous with a segmentally duplicated region of the Arabidopsis thaliana genome (Town et al. 2006). Nonetheless, some gene families are preferentially retained, which suggests that they are important in plant-specific adaptations (Blanc and Wolfe 2004; Shiu et al. 2004; Shiu et al. 2005). The two clades of Brassicaceae discussed above differ in ploidy level, with the Brassica/Raphanus clade having undergone a genome triplication after having diverged from the clade containing Arabidopsis and Capsella. Because of the higher rate of gene duplication in plants compared to other organisms, independent gene losses have also occurred at higher rates, which obscure orthologous relationships. With Raphanus cDNA sequences in hand, phylogenomic approaches can be applied to infer gene gain and loss events in gene families to provide a better understanding of the factors that contribute to duplicate gene retention. Raphanus diverged from Brassica only ~1-2 million years ago. Therefore, having Raphanus sequences would facilitate comparative studies of the consequences of polyploidy at a much shorter time scale than has been possible previously. The broad and deep knowledge of adaptive traits in Raphanus discussed above should facilitate making the link between the genes that are preferentially retained and adaptation to the natural environment.


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