Abstract
Fluorescence in situ hybridization (FISH) was developed more than 30 years ago and has been the most paradigm-changing technique in cytogenetic research. FISH has been used to answer questions related to structure, mutation, and evolution of not only individual chromosomes but also entire genomes. FISH has served as an important tool for chromosome identification in many plant species. This review intends to summarize and discuss key technical development and applications of FISH in plants since 2006. The most significant recent advance of FISH is the development and application of probes based on synthetic oligonucleotides (oligos). Oligos specific to a repetitive DNA sequence, to a specific chromosomal region, or to an entire chromosome can be computationally identified, synthesized in parallel, and fluorescently labeled. Oligo probes designed from conserved DNA sequences from one species can be used among genetically related species, allowing comparative cytogenetic mapping of these species. The advances with synthetic oligo probes will significantly expand the applications of FISH especially in non-model plant species. Recent achievements and future applications of FISH and oligo-FISH are discussed.
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Introduction
FISH has been the most important technique in plant cytogenetic research. DNA/RNA associated with a specific genomic region or an entire chromosome can be visualized by FISH on a range of cytological specimens. FISH was developed in the early 1980s (Langer-Safer et al. 1982) and became popular in the 1990s, owing to the introduction of CCD camera and imaging process of FISH signals. Searches using the keyword “fluorescence in situ hybridization” in the Web of Science database show a steady number of publications using FISH over the last 10 years (Fig. 1). Thus, FISH techniques will continue to play an important role in cytogenetic and genome research.
FISH was introduced in plants nearly 30 years ago (Leitch et al. 1991; Schwarzacher et al. 1989). Early development and applications of FISH in plants have been reviewed previously (Jiang and Gill 1994, 2006). In this review, I will discuss the advances in FISH since 2006 with a focus on recent developments using synthetic oligonucleotide (oligo) probes.
Recent development of the FISH techniques
Development of FISH probes based on synthetic oligos
Successful and efficient FISH experiments primarily rely on robust DNA probes. Repetitive DNA sequences and large-insert genomic DNA clones, such as bacterial artificial chromosome (BAC) clones, have been the most common FISH probes in plants (Jiang and Gill 1994, 2006). An important recent development is the application of FISH probes based on synthetic oligos. Oligo-based probes can be designed either from repetitive DNA elements or from single-copy DNA sequences, a paradigm shift from the traditional FISH probes using cloned DNA sequences.
Oligo probes designed from simple-sequence repeats or satellite repeats
Synthetic oligo-FISH probes were first developed to physically map simple-sequence repeats (SSRs) in plants. Oligos with repeated di-, tri-, or tetra-nucleotide motifs, such as (AG)12 or (AGG)5, were synthesized and used as FISH probes. These synthetic oligos can be end-labeled with biotin-dUTP or digoxigenin-dUTP (Cuadrado and Schwarzacher 1998; Schmidt and HeslopHarrison 1996), or are conjugated with a fluorochrome during synthesis (Danilova et al. 2012). The initial goals of FISH mapping of SSR-related oligos were to investigate the chromosomal organization of SSRs in plant genomes (Cuadrado and Schwarzacher 1998; Gortner et al. 1998; Schmidt and HeslopHarrison 1996). However, some of the SSR-related oligo probes produced distinct FISH signal patterns on individual chromosomes, which can be used for chromosome identification. For example, the FISH signals derived from the GAA repeats resemble the N-banding patterns on wheat and barley chromosomes (Danilova et al. 2012; Pedersen et al. 1996). Thus, SSR-related oligo probes have been used for chromosome identification in a number of plant species (Amosova et al. 2015; Carmona et al. 2013; Cuadrado and Jouve 2007; Danilova et al. 2012; Dou et al. 2009; Fuchs et al. 1998; Pedersen and Langridge 1997; Ruban and Badaeva 2018; Zheng et al. 2016).
Satellite repeats, or tandem repeats, are popular FISH probes in plants because the FISH signals derived from such repeats can often be used for chromosome identification (Jiang and Gill 1994, 2006). If a short sequence motif unique to a satellite repeat can be identified, an oligo probe based on this motif can be synthesized for FISH (Danilova et al. 2012; Fu et al. 2015; Tang et al. 2016, 2014). Such short synthetic probes may allow to distinguish and visualize subfamilies of a satellite repeat, and offer several advantages compared to traditionally prepared probes from cloned satellite repeats, including consistent probe quality and reduction of time and cost for probe preparation. In addition, denaturation of the chromosomal DNA is not required in FISH with some of these probes (Fu et al. 2015; Tang et al. 2016), which can positively impact the quality of FISH results. Synthetic oligo probes can be designed directly from computationally identified satellite repeats from genomic sequence data (Lang et al. 2018; Waminal et al. 2018). Thus, a fully sequenced reference genome is not required to develop such probes.
Oligo probes designed from single-copy DNA sequences
Oligo probes can also be designed from single-copy DNA sequences. Although a large number of single-copy oligos may be required to visualize a specific chromosomal region (Beliveau et al. 2012; Boyle et al. 2011; Yamada et al. 2011), oligos specific to a chromosomal region or to an entire chromosome can be computationally identified and synthesized in parallel as a pool (Beliveau et al. 2012; Han et al. 2015). Each oligo in the pool can be added with sequence tags at both ends during synthesis, which allows PCR-based amplification of the entire pool (Beliveau et al. 2012; Han et al. 2015). Subsequently, FISH probes can be generated from the pool via amplification of oligos labeled directly with a fluorochrome or indirectly with biotin-dUTP or digoxigenin-dUTP (Albert et al. 2019; Beliveau et al. 2012; Han et al. 2015). Thus, each synthesized oligo pool can be used as an infinite probe resource since the synthesized DNA (< 500 ng) can be used for up to a million FISH applications (Han et al. 2015).
Fine-tuning of the FISH procedure
The basic procedure of FISH was developed in 1982 (Langer-Safer et al. 1982) and has essentially remained unchanged in modern FISH protocols. Nevertheless, plant labs have continued to fine-tune the procedure to improve the sensitivity of the technique for detecting small DNA probes. Early reports on FISH mapping of DNA probes as small as few kilobases (kb) were rare (Jiang and Gill 1994, 2006) and the results were sometimes controversial. However, several plant labs have recently demonstrated routine detection of small DNA probes, mostly in the range of few kilobases (Aliyeva-Schnorr et al. 2015a; Danilova et al. 2017; Danilova and Birchler 2008; Danilova et al. 2012; Khrustaleva et al. 2016; Kirov et al. 2014b; Lamb et al. 2007; Li et al. 2018b; Lou et al. 2014; Nani et al. 2018; Said et al. 2018; Tiwari et al. 2015; Yu et al. 2007; Zhao et al. 2017).
The increased sensitivity of the FISH techniques is at least partly due to the improvement of plant chromosome preparation. Several modified chromosome preparation techniques have been reported in different plant species (Aliyeva-Schnorr et al. 2015b; Dang et al. 2015; Kato et al. 2006; Kirov et al. 2014a; Kuo et al. 2016; Setiawan et al. 2018; Yu et al. 2007). Various modifications have been implemented in these new techniques, which although minor, can positively impact the digestion of plant cell walls, reduce cytoplasm background, and maintain chromosome morphology, which may ultimately enhance the sensitivity of FISH. Nevertheless, although FISH mapping of DNA probes < 1 kb was reported (Khrustaleva et al. 2016), these probes can usually only be detected in a low percentage of cells and are not robust markers for routine chromosome identification or cytogenetic studies.
Recent applications of FISH in plant cytogenetic and genome research
The most common application of FISH is mapping DNA probes to chromosomes, thus allowing establishment of a physical map of the probes. If the DNA probes are genetically mapped, FISH mapping of these probes would allow integration of genetic linkage maps with chromosomal maps. These common applications of FISH were reviewed previously (Jiang and Gill 1994, 2006). Thus, I will only discuss the new applications of FISH since 2006.
Identification and validation of satellite repeats in plant genomes
Repetitive DNA elements can be cataloged as dispersed repeats, which are distributed throughout the genome, or satellite repeats, which are organized as tandem arrays and located in distinct region(s) on one or multiple chromosome(s). Satellite repeats are often the main DNA components in the centromeric and subtelomeric regions in plant genomes (Sharma and Raina 2005) and are the most popular probe resource for chromosome identification and cytogenetic studies in plants (Jiang and Gill 1994, 2006). The traditional approach of cloning and characterizing satellite repeats is tedious and time-consuming. RepeatExplorer (http://repeatexplorer.org/), a graph-based sequence clustering program, was developed for de novo identification of various types of repetitive DNA elements (Novak et al. 2010, 2013). A set of random shotgun genomic sequences from a target species is the only required resource for RepeatExplorer. Putative satellite repeats can be predicted based on their unique graphic characteristics. However, the predicted repeats need to be confirmed by FISH analysis. A combination of RepeatExplorer and FISH has become a popular methodology to identify and characterize major satellite repeats in many plant species (Belyayev et al. 2018; Camacho et al. 2015; Dluhosova et al. 2018; He et al. 2015; Heitkam et al. 2015; Iwata-Otsubo et al. 2016; Kirov et al. 2017; Macas et al. 2011; Perumal et al. 2017; Puterova et al. 2017; Ribeiro et al. 2017; Robledillo et al. 2018; Ruiz-Ruano et al. 2016; Torres et al. 2011; Yang et al. 2017).
One important application of RepeatExplorer and FISH is to uncover repeats associated with the centromeres of plant chromosomes. Centromeres in higher eukaryotes are marked with a centromere-specific histone H3 variant, CENH3, and are often composed of long arrays of repetitive DNA elements (Henikoff et al. 2001; Jiang et al. 2003). Centromeric DNA can be identified by chromatin immunoprecipitation (ChIP) using anti-CENH3 antibodies followed by sequencing of the immunoprecipitated DNA (ChIP-seq) (Yan et al. 2008). Repetitive DNA elements within the ChIP-seq data can be identified using RepeatExplorer. In addition, the relative enrichment of each computationally identified repeat in the ChIPed DNA versus a random genomic DNA sequence dataset would predict if each repeat is enriched in centromeres. The predicted centromere-specific repeats can then be confirmed by FISH (Gong et al. 2012; Neumann et al. 2012). This methodology allows identification of all centromeric repeats in a single experiment and has been successfully demonstrated in a number of plant species (Han et al. 2016; Kowar et al. 2016; Li et al. 2018a; Marques et al. 2015; Nagaki et al. 2015; Robledillo et al. 2018; Yang et al. 2018; Zhang et al. 2014; Zhang et al. 2017).
FISH-based assays of chromosome synteny and evolution
Comparative genetic linkage mapping with a common set of DNA markers was the traditional methodology to study the synteny and evolution of homoeologous chromosomes from different species (Paterson et al. 2000). This methodology, however, is time-consuming and relies on established mapping populations. Comparative FISH mapping of a common set of DNA probes provides an alternative method to reveal the synteny of homoeologous chromosomes in different species. The FISH-based approach is highly complementary to linkage mapping since it does not require a population and can be accomplished in a relatively short time.
Comparative FISH mapping of BAC clones developed in potato (Solanum tuberosum) or tomato (Solanum lycopersicum) was conducted in a number of Solanum species (Gaiero et al. 2017; Iovene et al. 2008; Lou et al. 2010; Szinay et al. 2012; Tang et al. 2008). Many of the potato and tomato BACs generated distinct FISH signals on distantly related Solanum species, including eggplant (Solanum melongena), which diverged from potato/tomato nearly 12 million years (Mys) ago (Doganlar et al. 2002). Mapping of a common set of BACs on meiotic pachytene chromosomes in different species was demonstrated to be a highly efficient approach to reveal the evolution of individual Solanum chromosomes in the last 12 million years (Lou et al. 2010; Szinay et al. 2012). Similarly, BAC-based comparative FISH mapping has been reported in a number of other plant species (Betekhtin et al. 2014; Han et al. 2009; Idziak et al. 2014; Iovene et al. 2011; Lysak et al. 2006, 2005; Vasconcelos et al. 2015).
BACs are valuable probe resources for comparative FISH mapping. However, BACs from plant species with large complex genomes, such as wheat, often contain a high percentage of repetitive DNA sequences and cannot be used for FISH mapping (Janda et al. 2006; Zhang et al. 2004). Instead, comparative FISH mapping can be performed using single-copy DNA probes in these plants (Aliyeva-Schnorr et al. 2016; Danilova et al. 2012, 2014). For example, a large number of single-copy cDNA probes from wheat were used for FISH mapping in various related diploid and polyploid species (Danilova et al. 2017, 2012, 2014; Said et al. 2018). The comparative FISH mapping results revealed the evolution of several known translocations within the A genome chromosomes of wheat (Danilova et al. 2012) and detected several new chromosome rearrangements in the wild species (Danilova et al. 2017, 2014; Said et al. 2018).
FISH-based assays on gene duplication and amplification
Gene duplication is a common molecular mechanism for adaptation to a changing environment (Kondrashov 2012). Tandem duplication resulting from unequal crossover is the most common type of gene duplication and can be readily analyzed using traditional molecular methods. However, it is often difficult to characterize complex or massive duplication/amplification of a gene or a gene cluster. FISH can be a powerful tool to analyze such duplication/amplification events.
Overexpression of the 5-enolpyruvylshikimate-3-phosphate synthase (EPSPS) gene can render crops resistant to the herbicide glyphosate. Unfortunately, many weeds have developed resistance to glyphosate due to extensive application of this herbicide. Duplication or amplification of the EPSPS gene is a common and naturally occurring mechanism for the acquired resistance in glyphosate-tolerant weeds (Ngo et al. 2018; Powles 2010; Salas et al. 2012; Zhang et al. 2015). Interestingly, the duplication mode of the EPSPS gene is different among glyphosate-resistant weeds. For example, the copy number of the EPSPS gene in glyphosate-resistant Amaranthus tuberculatus and Kochia scoparia plants ranged from a few copies up to 16 copies, and the duplications were likely derived from the classical “unequal crossover” mechanism based on the FISH signal patterns of the EPSPS gene on the target chromosomes as well as on DNA fibers (Dillon et al. 2017; Jugulam et al. 2014). FISH mapping also revealed that the EPSPS gene escaped to an extra chromosome in A. tuberculatus (Dillon et al. 2017). This extra chromosome was likely derived from the original EPSPS-carrying chromosome via rearrangements (Koo et al. 2018a). The copy number of the EPSPS gene in glyphosate-resistant Amaranthus palmeri plants can reach up to 160 (Gaines et al. 2010). FISH mapping revealed that the amplified EPSPS genes were dispersed along all chromosomes, indicating that the amplification was not derived from unequal crossovers (Gaines et al. 2010). Strikingly, a recent FISH-based study revealed that the amplification of the EPSPS gene in A. palmeri was based on a 297-kb extrachromosomal circular DNA (eccDNA) molecule. The eccDNAs are transmitted through mitosis and meiosis by an unknown mechanism of tethering to chromosomes (Koo et al. 2018b).
The niche applications of fiber-FISH
FISH can be applied to DNA molecules spread on glass slides (Fransz et al. 1996; Jackson et al. 1999, 1998). Fiber-FISH were mostly used to analyze the structure and organization of repetitive DNA sequences and to measure the length of long DNA molecules (Jiang and Gill 2006). Another unique value of fiber-FISH is the analysis of tandem duplications associated with large genomic duplicons. An early example was the fiber-FISH characterization of a 620-kb mitochondrial DNA (mtDNA) fragment inserted in chromosome 2 of Arabidopsis thaliana (Stupar et al. 2001). This large mtDNA insert was derived from complex duplication and deletion events (Stupar et al. 2001), which could not be characterized using traditional methods, such as PCR or Southern blot hybridization.
Fiber-FISH has continued to be a valuable technique to characterize large complex DNA loci. For example, the soybean cyst nematode (SCN) resistance locus Rhg1 was mapped to a 31-kb region spanning several different genes (Cook et al. 2012). This 31-kb DNA segment occurs as a single copy in SCN-susceptible lines, but is present with multiple copies in SCN-resistant lines. The copy numbers of this 31-kb duplicon were unambiguously visualized by fiber-FISH (Cook et al. 2014, 2012). Fiber-FISH can also be used to visualize circular DNA molecules (Koo et al. 2018b) as well as artificially assembled long linear DNA molecules (Lin et al. 2011). In addition, fiber-FISH can be combined with immunodetection of methylated cytosine on DNA fibers. Combining these two techniques allows mapping DNA methylation associated with repetitive DNA sequences (Koo et al. 2011; Lough et al. 2015), which cannot be accurately assessed by DNA sequencing–based techniques.
Future applications of oligo-FISH
Application of the FISH techniques has mainly been limited by the lack of robust DNA probes in most plant species, especially in non-model plants. Cloned DNA probes, such as BACs, are either not available or not useful in most plants. Thus, the recent development of FISH using synthetic oligo probes designed from single-copy DNA sequences will dramatically expand the applications of FISH in many plant species.
Development of oligo-FISH probes
Oligo-FISH probes can be designed from any plant species with a sequenced genome. Oligos specific to a specific region(s) of a chromosome or to an entire chromosome can be selected using the Chorus software (https://github.com/forrestzhang/Chorus). Several questions rise in designing probes for different plant species:
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1.
How to design a probe for plants without a reference genome? Since chromosome-specific oligos are selected from single-copy sequences, including genes, oligo probes designed from one species are likely useful in other related species. Indeed, the first oligo probes developed from cucumber (Cucumis sativus) produced excellent signals on chromosomes of melon (Cucumis melo) and other Cucumis species that diverged from cucumber up to 12 Mys ago (Han et al. 2015). Similarly, oligo probes designed from potato (Solanum tuberosum) showed high-quality FISH signals on chromosomes of tomato (S. lycopersicum) (Fig. 2A), which diverged from potato approximately 5–8 Mys ago (Braz et al. 2018). Nevertheless, the quality of FISH signals from heterologous probes will reduce as the genetic distance of the two species increases. Although potato oligo probes generated signals on eggplant (S. melongena) chromosomes, which diverged from a common ancestor of potato/tomato 15.5 Mys ago, the signals on eggplant chromosomes were weak and not as punctuated as those on potato chromosomes (Braz et al. 2018). To avoid the quality problem associated with heterologous probes, shotgun genomic sequences can be generated from a plant species and mapped to the reference genome of a related model species. Oligos can then be designed based on the sequence reads from the target species, rather than from a heterologous reference genome.
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2.
How to design a chromosome-specific probe in a polyploid species? Many plants are polyploids containing multiple genomes with various levels of homology. Thus, a probe designed from one chromosome will cross-hybridize with other homologous or homoeologous chromosome(s). In autopolyploids where multiple genomes are identical, such as potato (2n=4x=48), an oligo probe will generate identical FISH signals on all homologous chromosomes (Braz et al. 2018) (Fig. 2C). In allopolyploids, however, the level of cross-hybridization is correlated with the level of sequence similarity between the homoeologous chromosomes. We have recently tested the possibility to develop chromosome-specific probes in switchgrass (Panicum virgatum, 2n=4x=36), an allotetraploid species. We first designed a chromosome painting probe for switchgrass chromosome 8a. All 27,000 oligos were designed based on the sequence of chromosome 8a. Any oligos mapped to a second location (> 75% homology) were discarded to minimize the hybridization of the probe to chromosome 8b. This probe generated strong signals on chromosome 8a (Fig. 2D1), but very weak signals on chromosome 8b (Fig. 2D2). We then designed a chromosome painting probe for the short arms of both chromosomes 4a and 4b in switchgrass (Fig. 2E1). All 27,000 oligos were designed based on the sequence of chromosome 4a. Only the oligos that show > 90% sequence similarity to the sequences of chromosome 4b were selected to maximize the hybridization of the probe to both 4a and 4b. The FISH signals on chromosomes 4a and 4b showed a similar intensity (Fig. 2E2). Alternatively, each oligo can be designed to have a similar sequence similarity against all homoeologous chromosomes in an allopolyploid species. Such an oligo probe would hybridize with all homoeologous chromosomes with a similar level of signal intensity.
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3.
What is the appropriate oligo number/density of a probe? The number of oligos of an oligo-FISH probe is critical for the quality (intensity) of the FISH signals. In general, a probe with more oligos (or a higher density) will cost more but generate brighter signals (Fig. 2C). Our experience gained in several different plant species indicates that a density of 0.1–0.5 oligo/kb is sufficient to generate high-quality whole-chromosome painting signals on condensed metaphase chromosomes. Pachytene chromosomes can be extended 10–20 times longer than somatic metaphase chromosomes. Thus, a higher oligo density is recommended if the probe will be used for painting meiotic pachytene chromosomes. A rice chromosome 9 probe with a density of 2/kb showed excellent signals on pachytene chromosomes (Hou et al. 2018). A potato chromosome 11 probe with a density of 0.6/kb was sufficient to visualize the entire pachytene chromosomes (Fig. 2F). However, if the oligo probe is designed to visualize a small genomic region (< 10 kb), then the probe should include as many oligos as possible. Overlapping oligos and oligos targeting both strands of the corresponding DNA sequence can be incorporated to maximize the FISH signal strength of the probe.
Chromosome identification and karyotyping
An oligo-FISH barcode system was recently developed as a new tool for chromosome identification in potato and related Solanum species (Braz et al. 2018). In this system, two oligo probes were designed from one or multiple regions, or “spots,” on every chromosome. Thus, the FISH signals derived from the two probes resemble a chromosome banding pattern, or a “barcode” that uniquely labels each of the 12 potato chromosomes (Braz et al. 2018) (Fig. 2A). This FISH barcode allowed identification of every chromosome in cultivated potato (2n=4x=48) as well as in Solanum demissum (2n=6x=72), a hexaploid wild species (Fig. 2B). Remarkably, the same barcode can be used to identify the 12 homoeologous chromosomes among distantly related Solanum species, including tomato and eggplant (Braz et al. 2018).
For most plant species, identification of all chromosomes in a single metaphase cell has not been possible. Although FISH-based chromosome identification systems using BAC or repetitive DNA probes were developed in several plant species (Jiang and Gill 2006), these systems are time-consuming to develop and/or cannot be applied to other plant species, especially to plants with smaller chromosomes or species with a large number of chromosomes. The oligo-FISH barcode system has the potential to become a universal system for plant chromosome identification. Nevertheless, we anticipate a few technical challenges for some plant species. (1) Plants with a large number of small chromosomes. The sizes of potato chromosomes range from 45 to 89 Mb. Since the distance between two “spots” needs to be separated by 5–10 Mb to ensure consistent separation of the FISH signals, only a single spot may be designed on some of the short potato chromosomal arms (Fig. 2A). If a plant species has smaller but more chromosomes than potato, it may not be possible to develop a similar two-color FISH barcode and additional probes (colors) may be required to cover all chromosomes. (2) Plants with very large genomes. To ensure strong and punctuated signals, each “spot” should include ~ 1000 oligos that are restricted within a relatively small chromosomal region (these regions span 184–707 kb in potato (Braz et al. 2018)). Such chromosomal regions may not be common in plants with very large genomes, such as wheat, which contains > 90% repetitive DNA sequences.
Although karyotypes have been developed in many plant species, individual chromosomes were not identified in most reported karyotypes. Therefore, these karyotypes are expected to be error-prone due to chromosome misidentification and are not comparable to those of related species. The oligo-FISH barcode system allows unambiguous development of karyotypes based on individually identified chromosomes, which can be used for comparative analysis (Braz et al. 2018). Modifications to the FISH barcode among related species would indicate putative chromosomal rearrangement and evolution. Two reciprocal chromosomal translocations were discovered in S. etuberosum and S. caripense, respectively, based on comparative karyotyping (Braz et al. 2018). The oligo-FISH barcode system will allow karyotyping of a large number of accessions or ecotypes within a species and studies of chromosome-scale genetic adaptation and evolution.
Applications of chromosome painting in different plant species
Painting of individual chromosomes has been impossible for most plant species due to the lack of methods to develop chromosome-specific DNA probes (Schubert et al. 2001). Chromosome painting has only been accomplished in A. thaliana and Brachypodium distachyon, both with very small genomes, by pooling a large number of repeat-free BACs derived from a specific chromosome as a FISH probe (Idziak et al. 2011; Lysak et al. 2001). The oligo-based chromosome painting technique should be applicable to any plant species with a sequenced genome (Han et al. 2015). This technique has already been successfully applied to a number of plant species, including cucumber (Han et al. 2015), strawberry (Qu et al. 2017), Aquilegia coerulea (Filiault et al. 2018), potato (Braz et al. 2018; He et al. 2018), rice (Hou et al. 2018), poplar (Xin et al. 2018), sugarcane (Meng et al. 2018), and maize (Albert et al. 2019). The maize genome contains a high percentage of repetitive DNA sequences derived from various types of complete and decayed transposable elements. Chromosome painting probes on all 10 maize chromosomes showed high specificity (Albert et al. 2019), indicating effective elimination of repeats during oligo selection using the Chorus software.
Chromosome painting can be applied to various cytogenetic and genome research in plants, including chromosomal evolution based on cross-species painting (Braz et al. 2018; Filiault et al. 2018; Han et al. 2015), characterization of cytogenetic stocks (Albert et al. 2019; Hou et al. 2018), monitoring chromosome pairing and transmission in meiosis (He et al. 2018) (Fig. 2E), and examining the quality of genomic sequence assembly (Xin et al. 2018). We expect an increasing number of new applications of this technique in different plant species.
Conclusions and future directions
FISH has been the most important technique in plant cytogenetic research since the 1990s. Few techniques have dominated a research field for more than 30 years. Unfortunately, the application of FISH techniques has been hindered by the lack of robust DNA probes in many plant species, especially non-model plant species with no or limited genomic resources. This obstacle, however, is significantly alleviated by application of synthetic oligo probes. Thus, we expect a significant expansion of FISH applications in plants. Several exciting new developments of FISH have recently been reported in model animal species. For example, CAS-FISH used a fluorescently labeled nuclease-deficient Cas9 (dCas9) proteins to label and detect genomic regions in mammalian cells without using a DNA-denaturing step that would disturb the nuclear genomic organization of fixed or living cells (Deng et al. 2015). Single-molecule RNA-FISH (smRNA-FISH) techniques have been developed to measure transcription of multiple genes or non-coding RNAs within single cells (Cabili et al. 2015; Lubeck and Cai 2012). We expect adaption and application of some of these new FISH techniques in plants (Dreissig et al. 2017; Duncan et al. 2016; Fujimoto et al. 2016). Nevertheless, chromosome-based FISH experiments will continue to be the primary application in plants and oligo-based synthetic probes will become a cornerstone methodology in the future.
Abbreviations
- BAC:
-
Bacterial artificial chromosome
- ChIP:
-
Chromatin immunoprecipitation
- eccDNA:
-
Extrachromosomal circular DNA
- FISH:
-
Fluorescence in situ hybridization
- Mys:
-
Million years
- Oligo:
-
Oligonucleotide
- SSR:
-
Simple-sequence repeats
References
Albert PS, Zhang T, Semrau K, Rouillard J-M, Kao Y-H, Wang C-JR, Danilova TV, Jiang JM, Birchler JA (2019) Whole-chromosome paints in maize reveal rearrangements, nuclear domains, and chromosomal relationships. Proc Natl Acad Sci U S A 116:1679–1685
Aliyeva-Schnorr L, Beier S, Karafiatova M, Schmutzer T, Scholz U, Dolezel J, Stein N, Houben A (2015a) Cytogenetic mapping with centromeric bacterial artificial chromosomes contigs shows that this recombination-poor region comprises more than half of barley chromosome 3H. Plant J 84:385–394
Aliyeva-Schnorr L, Ma L, Houben A (2015b) A fast air-dry dropping chromosome preparation method suitable for FISH in plants. J Vis Exp:e53470
Aliyeva-Schnorr L, Stein N, Houben A (2016) Collinearity of homoeologous group 3 chromosomes in the genus Hordeum and Secale cereale as revealed by 3H-derived FISH analysis. Chromosom Res 24:231–242
Amosova AV, Bolsheva NL, Samatadze TE, Twardovska MO, Zoshchuk SA, Andreev IO, Badaeva ED, Kunakh VA, Muravenko OV (2015) Molecular cytogenetic analysis of Deschampsia antarctica Desv. (Poaceae), maritime antarctic. Plos One 10:e0138878
Beliveau BJ, Joyce EF, Apostolopoulos N, Yilmaz F, Fonseka CY, McCole RB, Chang YM, Li JB, Senaratne TN, Williams BR, Rouillard JM, Wu CT (2012) Versatile design and synthesis platform for visualizing genomes with Oligopaint FISH probes. Proc Natl Acad Sci U S A 109:21301–21306
Belyayev A, Pastova L, Fehrer J, Josefiova J, Chrtek J, Mraz P (2018) Mapping of Hieracium (Asteraceae) chromosomes with genus-specific satDNA elements derived from next-generation sequencing data. Plant Syst Evol 304:387–396
Betekhtin A, Jenkins G, Hasterok R (2014) Reconstructing the evolution of Brachypodium genomes using comparative chromosome painting. PLoS One 9:e115108
Boyle S, Rodesch MJ, Halvensleben HA, Jeddeloh JA, Bickmore WA (2011) Fluorescence in situ hybridization with high-complexity repeat-free oligonucleotide probes generated by massively parallel synthesis. Chromosom Res 19:901–909
Braz GT, He L, Zhao H, Zhang T, Semrau K, Rouillard JM, Torres GA, Jiang JM (2018) Comparative oligo-FISH mapping: an efficient and powerful methodology to reveal karyotypic and chromosomal evolution. Genetics 208:513–523
Cabili MN, Dunagin MC, McClanahan PD, Biaesch A, Padovan-Merhar O, Regev A, Rinn JL, Raj A (2015) Localization and abundance analysis of human IncRNAs at single-cell and single-molecule resolution. Genome Biol 16:20
Camacho JPM, Ruiz-Ruano FJ, Martin-Blazquez R, Lopez-Leon MD, Cabrero J, Lorite P, Cabral-de-Mello DC, Bakkali M (2015) A step to the gigantic genome of the desert locust: chromosome sizes and repeated DNAs. Chromosoma 124:263–275
Carmona A, Friero E, de Bustos A, Jouve N, Cuadrado A (2013) Cytogenetic diversity of SSR motifs within and between Hordeum species carrying the H genome: H-vulgare L. and H-bulbosum L. Theor Appl Genet 126:949–961
Cook DE, Lee TG, Guo XL, Melito S, Wang K, Bayless AM, Wang JP, Hughes TJ, Willis DK, Clemente TE, Diers BW, Jiang JM, Hudson ME, Bent AF (2012) Copy number variation of multiple genes at Rhg1 mediates nematode resistance in soybean. Science 338:1206–1209
Cook DE, Bayless AM, Wang K, Guo XL, Song QJ, Jiang JM, Bent AF (2014) Distinct copy number, coding sequence, and locus methylation patterns underlie Rhg1-mediated soybean resistance to soybean cyst nematode. Plant Physiol 165:630–647
Cuadrado A, Jouve N (2007) The nonrandom distribution of long clusters of all possible classes of trinucleotide repeats in barley chromosomes. Chromosom Res 15:711–720
Cuadrado A, Schwarzacher T (1998) The chromosomal organization of simple sequence repeats in wheat and rye genomes. Chromosoma 107:587–594
Dang JB, Zhao Q, Yang X, Chen Z, Xiang SQ, Liang GL (2015) A modified method for preparing meiotic chromosomes based on digesting pollen mother cells in suspension. Mol Cytogenet 8:80
Danilova TV, Birchler JA (2008) Integrated cytogenetic map of mitotic metaphase chromosome 9 of maize: resolution, sensitivity, and banding paint development. Chromosoma 117:345–356
Danilova TV, Friebe B, Gill BS (2012) Single-copy gene fluorescence in situ hybridization and genome analysis: Acc-2 loci mark evolutionary chromosomal rearrangements in wheat. Chromosoma 121:597–611
Danilova TV, Friebe B, Gill BS (2014) Development of a wheat single gene FISH map for analyzing homoeologous relationship and chromosomal rearrangements within the Triticeae. Theor Appl Genet 127:715–730
Danilova TV, Akhunova AR, Akhunov ED, Friebe B, Gill BS (2017) Major structural genomic alterations can be associated with hybrid speciation in Aegilops markgrafii (Triticeae). Plant J 92:317–330
Deng WL, Shi XH, Tjian R, Lionnet T, Singer RH (2015) CASFISH: CRISPR/Cas9-mediated in situ labeling of genomic loci in fixed cells. Proc Natl Acad Sci U S A 112:11870–11875
Dillon A, Varanasi VK, Danilova TV, Koo DH, Nakka S, Peterson DE, Tranel PJ, Friebe B, Gill BS, Jugulam M (2017) Physical mapping of amplified copies of the 5-enolpyruvylshikimate-3-phosphate synthase gene in glyphosate-resistant Amaranthus tuberculatus. Plant Physiol 173:1226–1234
Dluhosova J, Istvanek J, Nedelnik J, Repkova J (2018) Red clover (Trifolium pratense) and zigzag clover (T. medium) - a picture of genomic similarities and differences. Front Plant Sci 9:724
Doganlar S, Frary A, Daunay MC, Lester RN, Tanksley SD (2002) A comparative genetic linkage map of eggplant (Solanum melongena) and its implications for genome evolution in the Solanaceae. Genetics 161:1697–1711
Dou QW, Chen ZG, Liu YA, Tsujimoto H (2009) High frequency of karyotype variation revealed by sequential FISH and GISH in plateau perennial grass forage Elymus nutans. Breed Sci 59:651–656
Dreissig S, Schiml S, Schindele P, Weiss O, Rutten T, Schubert V, Gladilin E, Mette MF, Puchta H, Houben A (2017) Live-cell CRISPR imaging in plants reveals dynamic telomere movements. Plant J 91:565–573
Duncan S, Olsson TSG, Hartley M, Dean C, Rosa S (2016) A method for detecting single mRNA molecules in Arabidopsis thaliana. Plant Methods 12:13
Filiault DL, Ballerini ES, Mandáková T, Aköz G, Derieg NJ, Schmutz J, Jenkins J, Grimwood J, Shu S, Hayes RD, Hellsten U, Barry K, Yan J, Mihaltcheva S, Karafiátová M, Nizhynska V, Kramer EM, Lysak MA, Hodges SA, Nordborg M (2018) The Aquilegia genome provides insight into adaptive radiation and reveals an extraordinarily polymorphic chromosome with a unique history. eLife 7:e36426
Fransz PF, Alonso-Blanco C, Liharska TB, Peeters AJM, Zabel P, de Jong JH (1996) High-resolution physical mapping in Arabidopsis thaliana and tomato by fluorescence in situ hybridization to extended DNA fibres. Plant J 9:421–430
Fu SL, Chen L, Wang YY, Li M, Yang ZJ, Qiu L, Yan BJ, Ren ZL, Tang ZX (2015) Oligonucleotide probes for ND-FISH analysis to identify rye and wheat chromosomes. Sci Rep 5:10552
Fuchs J, Strehl S, Brandes A, Schweizer D, Schubert I (1998) Molecular-cytogenetic characterization of the Vicia faba genome - heterochromatin differentiation, replication patterns and sequence localization. Chromosom Res 6:219–230
Fujimoto S, Sugano SS, Kuwata K, Osakabe K, Matsunaga S (2016) Visualization of specific repetitive genomic sequences with fluorescent TALEs in Arabidopsis thaliana. J Exp Bot 67:6101–6110
Gaiero P, van de Belt J, Vilaro F, Schranz ME, Speranza P, de Jong H (2017) Collinearity between potato (Solanum tuberosum L.) and wild relatives assessed by comparative cytogenetic mapping. Genome 60:228–240
Gaines TA, Zhang WL, Wang DF, Bukun B, Chisholm ST, Shaner DL, Nissen SJ, Patzoldt WL, Tranel PJ, Culpepper AS, Grey TL, Webster TM, Vencill WK, Sammons RD, Jiang JM, Preston C, Leach JE, Westra P (2010) Gene amplification confers glyphosate resistance in Amaranthus palmeri. Proc Natl Acad Sci U S A 107:1029–1034
Gong ZY, Wu YF, Koblizkova A, Torres GA, Wang K, Iovene M, Neumann P, Zhang WL, Novak P, Buell CR, Macas J, Jiang JM (2012) Repeatless and repeat-based centromeres in potato: implications for centromere evolution. Plant Cell 24:3559–3574
Gortner G, Nenno M, Weising K, Zink D, Nagl W, Kahl G (1998) Chromosomal localization and distribution of simple sequence repeats and the Arabidopsis-type telomere sequence in the genome of Cicer arietinum L. Chromosom Res 6:97–104
Han YH, Zhang ZH, Liu CX, Liu JH, Huang SW, Jiang JM, Jin WW (2009) Centromere repositioning in cucurbit species: implication of the genomic impact from centromere activation and inactivation. Proc Natl Acad Sci U S A 106:14937–14941
Han YH, Zhang T, Thammapichai P, Weng YQ, Jiang JM (2015) Chromosome-specific painting in Cucumis species using bulked oligonucleotides. Genetics 200:771–779
Han JL, Masonbrink RE, Shan WB, Song FQ, Zhang JS, Yu WC, Wang KB, Wu YF, Tang HB, Wendel JF, Wang K (2016) Rapid proliferation and nucleolar organizer targeting centromeric retrotransposons in cotton. Plant J 88:992–1005
He QY, Cai ZX, Hu TH, Liu HJ, Bao CL, Mao WH, Jin WW (2015) Repetitive sequence analysis and karyotyping reveals centromere-associated DNA sequences in radish (Raphanus sativus L.). BMC Plant Biol 15:105
He L, Braz GT, Torres GA, Jiang JM (2018) Chromosome painting in meiosis reveals pairing of specific chromosomes in polyploid Solanum species. Chromosoma 127:505–513
Heitkam T, Petrasch S, Zakrzewski F, Kogler A, Wenke T, Wanke S, Schmidt T (2015) Next-generation sequencing reveals differentially amplified tandem repeats as a major genome component of Northern Europe’s oldest Camellia japonica. Chromosom Res 23:791–806
Henikoff S, Ahmad K, Malik HS (2001) The centromere paradox: stable inheritance with rapidly evolving DNA. Science 293:1098–1102
Hou LL, Xu M, Zhang T, Xu ZH, Wang WY, Zhang JX, Yu MM, Ji W, Zhu CW, Gong ZY, Gu MH, Jiang JM, Yu HX (2018) Chromosome painting and its applications in cultivated and wild rice. BMC Plant Biol 18:110
Idziak D, Betekhtin A, Wolny E, Lesniewska K, Wright J, Febrer M, Bevan MW, Jenkins G, Hasterok R (2011) Painting the chromosomes of Brachypodium - current status and future prospects. Chromosoma 120:469–479
Idziak D, Hazuka I, Poliwczak B, Wiszynska A, Wolny E, Hasterok R (2014) Insight into the karyotype evolution of Brachypodium species using comparative chromosome barcoding. PLoS One 9:e93503
Iovene M, Wielgus SM, Simon PW, Buell CR, Jiang JM (2008) Chromatin structure and physical mapping of chromosome 6 of potato and comparative analyses with tomato. Genetics 180:1307–1317
Iovene M, Cavagnaro PF, Senalik D, Buell CR, Jiang JM, Simon PW (2011) Comparative FISH mapping of Daucus species (Apiaceae family). Chromosom Res 19:493–506
Iwata-Otsubo A, Lin JY, Gill N, Jackson SA (2016) Highly distinct chromosomal structures in cowpea (Vigna unguiculata), as revealed by molecular cytogenetic analysis. Chromosom Res 24:197–216
Jackson SA, Wang ML, Goodman HM, Jiang JM (1998) Application of fiber-FISH in physical mapping of Arabidopsis thaliana. Genome 41:566–572
Jackson SA, Dong FG, Jiang JM (1999) Digital mapping of bacterial artificial chromosomes by fluorescence in situ hybridization. Plant J 17:581–587
Janda J, Safar J, Kubalakova M, Bartos J, Kovarova P, Suchankova P, Pateyron S, Cihalikova J, Sourdille P, Simkova H, Faivre-Rampant P, Hribova E, Bernard M, Lukaszewski A, Dolezel J, Chalhoub B (2006) Advanced resources for plant genomics: a BAC library specific for the short arm of wheat chromosome 1B. Plant J 47:977–986
Jiang JM, Gill BS (1994) Nonisotopic in situ hybridization and plant genome mapping: the first 10 years. Genome 37:717–725
Jiang JM, Gill BS (2006) Current status and the future of fluorescence in situ hybridization (FISH) in plant genome research. Genome 49:1057–1068
Jiang JM, Birchler JA, Parrott WA, Dawe RK (2003) A molecular view of plant centromeres. Trends Plant Sci 8:570–575
Jugulam M, Niehues K, Godar AS, Koo DH, Danilova T, Friebe B, Sehgal S, Varanasi VK, Wiersma A, Westra P, Stahlman PW, Gill BS (2014) Tandem amplification of a chromosomal segment harboring 5-enolpyruvylshikimate-3-phosphate synthase locus confers glyphosate resistance in Kochia scoparia. Plant Physiol 166:1200–1207
Kato A, Albert PS, Vega JM, Birchler JA (2006) Sensitive fluorescence in situ hybridization signal detection in maize using directly labeled probes produced by high concentration DNA polymerase nick translation. Biotech Histochem 81:71–78
Khrustaleva L, Jiang JM, Havey MJ (2016) High-resolution tyramide-FISH mapping of markers tightly linked to the male-fertility restoration (Ms) locus of onion. Theor Appl Genet 129:535–545
Kirov I, Divashuk M, Van Laere K, Soloviev A, Khrustaleva L (2014a) An easy “SteamDrop” method for high quality plant chromosome preparation. Mol Cytogenet 7:21
Kirov I, Van Laere K, De Riek J, De Keyser E, Van Roy N, Khrustaleva L (2014b) Anchoring linkage groups of the Rosa genetic map to physical chromosomes with Tyramide-FISH and EST-SNP markers. PLoS One 9:e95793
Kirov IV, Kiseleva AV, Van Laere K, Van Roy N, Khrustaleva LI (2017) Tandem repeats of Allium fistulosum associated with major chromosomal landmarks. Mol Gen Genomics 292:453–464
Kondrashov FA (2012) Gene duplication as a mechanism of genomic adaptation to a changing environment. Proc R Soc B Biol Sci 279:5048–5057
Koo DH, Han FP, Birchler JA, Jiang JM (2011) Distinct DNA methylation patterns associated with active and inactive centromeres of the maize B chromosome. Genome Res 21:908–914
Koo DH, Jugulam M, Putta K, Cuvaca IB, Peterson DE, Currie RS, Friebe B, Gill BS (2018a) Gene duplication and aneuploidy trigger rapid evolution of herbicide resistance in common waterhemp. Plant Physiol 176:1932–1938
Koo DH, Molin WT, Saski CA, Jiang JM, Putta K, Jugulam M, Friebe B, Gill BS (2018b) Extrachromosomal circular DNA-based amplification and transmission of herbicide resistance in crop weed Amaranthus palmeri. Proc Natl Acad Sci U S A 115:3332–3337
Kowar T, Zakrzewski F, Macas J, Koblizkova A, Viehoever P, Weisshaar B, Schmidt T (2016) Repeat composition of CenH3-chromatin and H3K9me2-marked heterochromatin in sugar beet (Beta vulgaris). BMC Plant Biol 16:120
Kuo YT, Hsu HL, Yeh CH, Chang SB (2016) Application of a modified drop method for high-resolution pachytene chromosome spreads in two Phalaenopsis species. Mol Cytogenet 9:44
Lamb JC, Danilova T, Bauer MJ, Meyer JM, Holland JJ, Jensen MD, Birchler JA (2007) Single-gene detection and karyotyping using small-target fluorescence in situ hybridization on maize somatic chromosomes. Genetics 175:1047–1058
Lang T, Li G, Wang H, Yu Z, Chen Q, Yang E, Fu S, Tang Z, Yang Z (2018) Physical location of tandem repeats in the wheat genome and application for chromosome identification. Planta. https://doi.org/10.1007/s00425-00018-03033-00424
Langer-Safer PR, Levine M, Ward DC (1982) Immunological method for mapping genes on Drosophila polytene chromosomes. Proc Natl Acad Sci U S A Biol Sci 79:4381–4385
Leitch IJ, Leitch AR, Heslopharrison JS (1991) Physical mapping of plant DNA sequences by simultaneous in situ hybridization of two differently labeled fluorescent probes. Genome 34:329–333
Li YJ, Zuo S, Zhang ZL, Li ZJ, Han JL, Chu ZQ, Hasterok R, Wang K (2018a) Centromeric DNA characterization in the model grass Brachypodium distachyon provides insights on the evolution of the genus. Plant J 93:1088–1101
Li Z, Bi YF, Wang X, Wang YZ, Yang SQ, Zhang ZT, Chen JF, Lou QF (2018b) Chromosome identification in Cucumis anguria revealed by cross-species single-copy gene FISH. Genome 61:397–404
Lin L, Koo DH, Zhang WL, St Peter J, Jiang JM (2011) De novo assembly of potential linear artificial chromosome constructs capped with expansive telomeric repeats. Plant Methods 7:10
Lou QF, Iovene M, Spooner DM, Buell CR, Jiang JM (2010) Evolution of chromosome 6 of Solanum species revealed by comparative fluorescence in situ hybridization mapping. Chromosoma 119:435–442
Lou QF, Zhang YX, He YH, Li J, Jia L, Cheng CY, Guan W, Yang SQ, Chen JF (2014) Single-copy gene-based chromosome painting in cucumber and its application for chromosome rearrangement analysis in Cucumis. Plant J 78:169–179
Lough AN, Faries KM, Koo DH, Hussain A, Roark LM, Langewisch TL, Backes T, Kremling KAG, Jiang JM, Birchler JA, Newton KJ (2015) Cytogenetic and sequence analyses of mitochondrial DNA insertions in nuclear chromosomes of maize. G3 5:2229–2239
Lubeck E, Cai L (2012) Single-cell systems biology by super-resolution imaging and combinatorial labeling. Nat Methods 9:743–748
Lysak MA, Fransz PF, Ali HBM, Schubert I (2001) Chromosome painting in Arabidopsis thaliana. Plant J 28:689–697
Lysak MA, Koch MA, Pecinka A, Schubert I (2005) Chromosome triplication found across the tribe Brassiceae. Genome Res 15:516–525
Lysak MA, Berr A, Pecinka A, Schmidt R, McBreen K, Schubert I (2006) Mechanisms of chromosome number reduction in Arabidopsis thaliana and related Brassicaceae species. Proc Natl Acad Sci U S A 103:5224–5229
Macas J, Kejnovsky E, Neumann P, Novak P, Koblizkova A, Vyskot B (2011) Next generation sequencing-based analysis of repetitive DNA in the model dioecious plant Silene latifolia. PLoS One 6:e27335
Marques A, Ribeiro T, Neumann P, Macas J, Novak P, Schubert V, Pellino M, Fuchs J, Ma W, Kuhlmann M, Brandt R, Vanzela ALL, Beseda T, Simkova H, Pedrosa-Harand A, Houben A (2015) Holocentromeres in Rhynchospora are associated with genome-wide centromere-specific repeat arrays interspersed among euchromatin. Proc Natl Acad Sci U S A 112:13633–13638
Meng Z, Zhang ZL, Yan TY, Lin QF, Wang Y, Huang WY, Huang YJ, Li ZJ, Yu QY, Wang JP, Wang K (2018) Comprehensively characterizing the cytological features of Saccharum spontaneum by the development of a complete set of chromosome-specific oligo probes. Front Plant Sci 9:1624
Nagaki K, Tanaka K, Yamaji N, Kobayashi H, Murata M (2015) Sunflower centromeres consist of a centromere-specific LINE and a chromosome-specific tandem repeat. Front Plant Sci 6:912
Nani TF, Schnable JC, Washburn JD, Albert P, Pereira WA, Sobrinho FS, Birchler JA, Techio VH (2018) Location of low copy genes in chromosomes of Brachiaria spp. Mol Biol Rep 45:109–118
Neumann P, Navratilova A, Schroeder-Reiter E, Koblizkova A, Steinbauerova V, Chocholova E, Novak P, Wanner G, Macas J (2012) Stretching the rules: monocentric chromosomes with multiple centromere domains. PLoS Genet 8:e1002777
Ngo TD, Malone JM, Boutsalis P, Gill G, Preston C (2018) EPSPS gene amplification conferring resistance to glyphosate in windmill grass (Chloris truncata) in Australia. Pest Manag Sci 74:1101–1108
Novak P, Neumann P, Macas J (2010) Graph-based clustering and characterization of repetitive sequences in next-generation sequencing data. BMC Bioinformatics 11:378
Novak P, Neumann P, Pech J, Steinhaisl J, Macas J (2013) RepeatExplorer: a galaxy-based web server for genome-wide characterization of eukaryotic repetitive elements from next-generation sequence reads. Bioinformatics 29:792–793
Paterson AH, Bowers JE, Burow MD, Draye X, Elsik CG, Jiang CX, Katsar CS, Lan TH, Lin YR, Ming RG, Wright RJ (2000) Comparative genomics of plant chromosomes. Plant Cell 12:1523–1539
Pedersen C, Langridge P (1997) Identification of the entire chromosome complement of bread wheat by two-colour FISH. Genome 40:589–593
Pedersen C, Rasmussen SK, LindeLaursen I (1996) Genome and chromosome identification in cultivated barley and related species of the Triticeae (Poaceae) by in situ hybridization with the GAA-satellite sequence. Genome 39:93–104
Perumal S, Waminal NE, Lee J, Lee J, Choi BS, Kim HH, Grandbastien MA, Yang TJ (2017) Elucidating the major hidden genomic components of the A, C, and AC genomes and their influence on Brassica evolution. Sci Rep 7:17986
Powles SB (2010) Gene amplification delivers glyphosate-resistant weed evolution. Proc Natl Acad Sci U S A 107:955–956
Puterova J, Razumova O, Martinek T, Alexandrov O, Divashuk M, Kubat Z, Hobza R, Karlov G, Kejnovsky E (2017) Satellite DNA and transposable elements in seabuckthorn (Hippophae rhamnoides), a dioecious plant with small Y and large X chromosomes. Genome Biol Evol 9:197–212
Qu MM, Li KP, Han YL, Chen L, Li ZY, Han YH (2017) Integrated karyotyping of woodland strawberry (Fragaria vesca) with oligopaint FISH probes. Cytogenet Genome Res 153:158–164
Ribeiro T, Marques A, Novak P, Schubert V, Vanzela ALL, Macas J, Houben A, Pedrosa-Harand A (2017) Centromeric and non-centromeric satellite DNA organisation differs in holocentric Rhynchospora species. Chromosoma 126:325–335
Robledillo LA, Koblizkova A, Novak P, Bottinger K, Vrbova I, Neumann P, Schubert I, Macas J (2018) Satellite DNA in Vicia faba is characterized by remarkable diversity in its sequence composition, association with centromeres, and replication timing. Sci Rep 8:5838
Ruban AS, Badaeva ED (2018) Evolution of the S-genomes in Triticum-Aegilops alliance: evidences from chromosome analysis. Front Plant Sci 9:1756
Ruiz-Ruano FJ, Lopez-Leon MD, Cabrero J, Camacho JPM (2016) High-throughput analysis of the satellitome illuminates satellite DNA evolution. Sci Rep 6:28333
Said M, Hribova E, Danilova TV, Karafiatova M, Cizkova J, Friebe B, Dolezel J, Gill BS, Vrana J (2018) The Agropyron cristatum karyotype, chromosome structure and cross-genome homoeology as revealed by fluorescence in situ hybridization with tandem repeats and wheat single-gene probes. Theor Appl Genet 131:2213–2227
Salas RA, Dayan FE, Pan ZQ, Watson SB, Dickson JW, Scott RC, Burgos NR (2012) EPSPS gene amplification in glyphosate-resistant Italian ryegrass (Lolium perenne ssp multiflorum) from Arkansas. Pest Manag Sci 68:1223–1230
Schmidt T, HeslopHarrison JS (1996) The physical and genomic organization of microsatellites in sugar beet. Proc Natl Acad Sci U S A 93:8761–8765
Schubert I, Fransz PF, Fuchs J, de Jong JH (2001) Chromosome painting in plants. Methods Cell Sci 23:57–69
Schwarzacher T, Leitch AR, Bennett MD, Heslopharrison JS (1989) In situ localization of parental genomes in a wide hybrid. Ann Bot (London) 64:315–324
Setiawan AB, Teo CH, Kikuchi S, Sassa H, Koba T (2018) An improved method for inducing prometaphase chromosomes in plants. Mol Cytogenet 11:32
Sharma S, Raina SN (2005) Organization and evolution of highly repeated satellite DNA sequences in plant chromosomes. Cytogenet Genome Res 109:15–26
Stupar RM, Lilly JW, Town CD, Cheng Z, Kaul S, Buell CR, Jiang JM (2001) Complex mtDNA constitutes an approximate 620-kb insertion on Arabidopsis thaliana chromosome 2: implication of potential sequencing errors caused by large-unit repeats. Proc Natl Acad Sci U S A 98:5099–5103
Szinay D, Wijnker E, van den Berg R, Visser RGF, de Jong H, Bai YL (2012) Chromosome evolution in Solanum traced by cross-species BAC-FISH. New Phytol 195:688–698
Tang XM, Szinay D, Lang C, Ramanna MS, van der Vossen EAG, Datema E, Lankhorst RK, de Boer J, Peters SA, Bachem C, Stiekema W, Visser RGF, de Jong H, Bai YL (2008) Crosss species bacterial artificial chromosome-fluorescence in situ hybridization painting of the tomato and potato chromosome 6 reveals undescribed chromosomal rearrangements. Genetics 180:1319–1328
Tang ZX, Yang ZJ, Fu SL (2014) Oligonucleotides replacing the roles of repetitive sequences pAs1, pSc119.2, pTa-535, pTa71, CCS1, and pAWRC.1 for FISH analysis. J Appl Genet 55:313–318
Tang SY, Qiu L, Xiao ZQ, Fu SL, Tang ZX (2016) New oligonucleotide probes for ND-FISH analysis to identify barley chromosomes and to investigate polymorphisms of wheat chromosomes. Genes-Basel 7:118
Tiwari VK, Wang SC, Danilova T, Koo DH, Vrana J, Kubalakova M, Hribova E, Rawat N, Kalia B, Singh N, Friebe B, Dolezel J, Akhunov E, Poland J, Sabir JSM, Gill BS (2015) Exploring the tertiary gene pool of bread wheat: sequence assembly and analysis of chromosome 5M(g) of Aegilops geniculata. Plant J 84:733–746
Torres GA, Gong ZY, Iovene M, Hirsch CD, Buell CR, Bryan GJ, Novak P, Macas J, Jiang JM (2011) Organization and evolution of subtelomeric satellite repeats in the potato genome. G3 1:85–92
Vasconcelos EV, Fonseca AFD, Pedrosa-Harand A, Bortoleti KCD, Benko-Iseppon AM, da Costa AF, Brasileiro-Vidal AC (2015) Intra- and interchromosomal rearrangements between cowpea [Vigna unguiculata (L.) Walp.] and common bean (Phaseolus vulgaris L.) revealed by BAC-FISH. Chromosom Res 23:253–266
Waminal NE, Pellerin RJ, Kim NS, Jayakodi M, Park JY, Yang TJ, Kim HH (2018) Rapid and efficient FISH using pre-labeled oligomer probes. Sci Rep 8:8224
Xin H, Zhang T, Han Y, Wu Y, Shi J, Xi M, Jiang JM (2018) Chromosome painting and comparative physical mapping of the sex chromosomes in Populus tomentosa and Populus deltoides. Chromosoma 127:313–321
Yamada NA, Rector LS, Tsang P, Carr E, Scheffer A, Sederberg MC, Aston ME, Ach RA, Tsalenko A, Sampas N, Peter B, Bruhn L, Brothman AR (2011) Visualization of fine-scale genomic structure by oligonucleotide-based high-resolution FISH. Cytogenet Genome Res 132:248–254
Yan HH, Talbert PB, Lee HR, Jett J, Henikoff S, Chen F, Jiang JM (2008) Intergenic locations of rice centromeric chromatin. PLoS Biol 6:2563–2575
Yang SQ, Qin XD, Cheng CY, Li Z, Lou QF, Li J, Chen JF (2017) Organization and evolution of four differentially amplified tandem repeats in the Cucumis hystrix genome. Planta 246:749–761
Yang XM, Zhao HN, Zhang T, Zeng ZX, Zhang PD, Zhu B, Han YH, Braz GT, Casler MD, Schmutz J, Jiang JM (2018) Amplification and adaptation of centromeric repeats in polyploid switchgrass species. New Phytol 218:1645–1657
Yu WC, Lamb JC, Han FP, Birchler JA (2007) Cytological visualization of DNA transposons and their transposition pattern in somatic cells of maize. Genetics 175:31–39
Zhang P, Li WL, Fellers J, Friebe B, Gill BS (2004) BAC-FISH in wheat identifies chromosome landmarks consisting of different types of transposable elements. Chromosoma 112:288–299
Zhang HQ, Koblizkova A, Wang K, Gong ZY, Oliveira L, Torres GA, Wu YF, Zhang WL, Novak P, Buell CR, Macas J, Jiang JM (2014) Boom-bust turnovers of megabase-sized centromeric DNA in Solanum species: rapid evolution of DNA sequences associated with centromeres. Plant Cell 26:1436–1447
Zhang C, Feng L, He TT, Yang CH, Chen GQ, Tian XS (2015) Investigating the mechanisms of glyphosate resistance in goosegrass (Eleusine indica) population from South China. J Integr Agric 14:909–918
Zhang WP, Zuo S, Li ZJ, Meng Z, Han JL, Song JQ, Pan YB, Wang K (2017) Isolation and characterization of centromeric repetitive DNA sequences in Saccharum spontaneum. Sci Rep 7:41659
Zhao HN, Zeng ZX, Koo DH, Gill BS, Birchler JA, Jiang JM (2017) Recurrent establishment of de novo centromeres in the pericentromeric region of maize chromosome 3. Chromosom Res 25:299–311
Zheng JS, Sun CZ, Zhang SN, Hou XL, Bonnema G (2016) Cytogenetic diversity of simple sequences repeats in morphotypes of Brassica rapa ssp chinensis. Front Plant Sci 7:1049
Acknowledgments
FISH images in Fig. 2 were developed by Guilherme Braz, Li He, Tao Zhang, and Pingdong Zhang.
Funding
Cytogenetic research in the author’s lab has been supported by National Science Foundation (NSF) grants IOS-1444514 and MCB-1412948.
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Jiang, J. Fluorescence in situ hybridization in plants: recent developments and future applications. Chromosome Res 27, 153–165 (2019). https://doi.org/10.1007/s10577-019-09607-z
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DOI: https://doi.org/10.1007/s10577-019-09607-z