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University of British Columbia Botanical Garden and Centre for Plant Research, and Department of Botany, University of British Columbia, Vancouver, British Columbia V6T1Z4, Canada
1 Corresponding author: Centre for Plant Research and Department of Botany, 6270 University Blvd., University of British Columbia, Vancouver, BC V6T1Z4, Canada.
E-mail: keitha{at}interchange.ubc.ca
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ABSTRACT |
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 TOP ABSTRACT MATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
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Hybridization between two plant species can result in changes in gene expression (reviewed in ADAMS 2007). Up- and downregulation of expression in hybrids compared to their parents has been shown in interspecific triploid Senecio hybrids (HEGARTY et al. 2005, 2006). Intraspecific hybridization between two cultivars, ecotypes, or accessions also can result in up- or downregulation of gene expression, as shown in recent studies of diploid and triploid maize hybrids (AUGER et al. 2005; GUO et al. 2006; STUPAR and SPRINGER 2006; SWANSON-WAGNER et al. 2006; MEYER et al. 2007; SPRINGER and STUPAR 2007b; STUPAR et al. 2007; UZAROWSKA et al. 2007) in diploid wheat and rice hybrids (WU et al. 2003; BAO et al. 2005; WANG et al. 2006, and in hybrids between ecotypes of Arabidopsis thaliana (VUYLSTEKE et al. 2005). Hybridization also can affect expression of individual alleles, although few studies have assayed allelic expression variation in diploid hybrids. Allelic expression differences of nonimprinted autosomal genes have been reported in interspecific hybrids of Drosophila (WITTKOPP et al. 2004), as well as intraspecific F1 hybrids of mice (COWLES et al. 2002) and Saccharomyces cerevisiae (RONALD et al. 2005). Recent studies of intraspecific maize hybrids have shown unequal expression of parental alleles, including silencing of one allele (GUO et al. 2003, 2004; STUPAR and SPRINGER 2006; SPRINGER and STUPAR 2007b; STUPAR et al. 2007). A study of an Adh gene in interspecific cotton F1 hybrids revealed organ-specific allelic silencing of this gene (ADAMS and WENDEL 2005). Despite recent progress allelic variation in gene expression remains poorly investigated for interspecific plant hybrids.
Allelic variation in gene expression may arise from cis- or trans-regulatory factors (WITTKOPP et al. 2004). Cis-regulators are genetically tightly linked to a gene and influence transcription in an allele-specific manner. In contrast, trans-regulators are located elsewhere in the genome and modify gene expression by interacting with cis-regulators. Following hybridization, genes under pure cis-regulation tend to show additive expression patterns, whereas those under trans-regulation can display either additive or nonadditive expression, depending on whether a dosage effect exists (STUPAR and SPRINGER 2006; SPRINGER and STUPAR 2007a). Cis- or trans-regulation can be inferred by comparing the ratios of species-specific transcripts between the F1 hybrids and the parental species (WITTKOPP et al. 2004). Genes with strict cis-regulation have the same bias of expression of two alleles in both the hybrid and the parents. Genes with strict trans-regulation display allelic bias in the parents but are expected to have equal levels of allelic expression in the hybrid. While pure cis-effects imply the preservation of parental regulatory function, differential expression between parents and hybrid due to trans-effects are caused by hybridization that brings two genomes together, allowing both alleles to be exposed to a common set of trans-elements.
Populus hybrids provide a promising plant system to study interspecific hybridization and its genetic and molecular consequences. There are 30–40 different Populus species worldwide, including the common North American species Populus trichocarpa (black cottonwood), P. deltoides (eastern cottonwood), P. nigra (Lombardy poplar), and P. tremuloides (aspen). Populus has become a model system for research on wood-forming plants. P. trichocarpa is the first (and currently only) tree for which the genome has been sequenced (TUSKAN et al. 2006) and it is one of only four flowering plant species with a sequenced genome at the present time (the others being A. thaliana, Oryza sativa, and Vitis vinifera). As a sustainable source for paper fiber and biofuel, Populus hybrids are important economic plants. Populus hybrids often show strong heterosis (BRADSHAW and STETTLER 1995; LI et al. 1998), and the study of molecular responses to hybridization may provide insights into heterosis of Populus hybrids.
Here we studied the allelic variation in gene expression levels using P. trichocarpa x P. deltoides interspecific F1 hybrids. The allele-specific expression for 30 genes in four independently formed hybrids was assayed. To investigate whether there are organ-specific differences in allelic expression, both leaves and stems were examined for the same genes. To determine if biased allelic expression was the result of hybridization or reflects differing expression levels in the parents, we compared the ratio of species-specific transcripts in an F1 hybrid vs. that in its parents, and the results have implications for cis- and trans-gene regulation.
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MATERIALS AND METHODS |
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The analysis of cis- and trans-regulatory variation was conducted using a P. trichocarpa x P. deltoides F1 hybrid and its parental clones, P. trichocarpa accession Nisqually-1 and P. deltoides accession ILL 101. The hybrid was originally from a plantation of P. trichocarpa x P. deltoides F1 hybrids that were derived from the same cross by Dan Carson from Scott Paper in Harrison Mills, British Columbia. The maternal parent P. trichocarpa was planted at the UBC Botanical Garden and the paternal parent P. deltoides was provided by Carl Douglas. Cuttings of all three genotypes were grown under common greenhouse conditions at the UBC Horticultural Greenhouse for several months before tissue sampling. Young leaves from the hybrid and the two parents were collected at the same time during May 2007. For each tissue sample, three replicates were harvested and frozen immediately in liquid nitrogen and stored at –80° until use.
Sequence database searches:
Gene sequences were obtained from NCBI and the whole-genome shotgun sequence database of the P. trichocarpa Nisqually-1 genome that was available from the Joint Genome Institute (http://genome.jgi-psf.org/poplar0/poplar0.home.html). Primers for PCR (supplemental Table 1 at http://www.genetics.org/supplemental/) were designed using Primer Premier 5.0 to amplify both genomic DNAs and cDNAs.
Extraction of nucleic acids and synthesis of cDNA:
DNAs were extracted by using QIAGEN (Valencia, CA) DNeasy plant mini kit. Total RNA extraction was performed as described previously (ADAMS et al. 2003). DNA and RNA concentrations and purities were measured by using a NanoDrop spectrophotometer. RNAs were treated with DNaseI (New England Biolabs, Beverly, MA) before reverse transcription. Single-stranded cDNA was synthesized from 500 ng of total RNA using M-MLV reverse transcriptase (Invitrogen, Carlsbad, CA) according to the manufacturer's protocol. As controls for DNA contamination, reactions were also performed without reverse transcriptase at the same time. For the cis- and trans-regulatory variation analysis, mixed cDNAs were synthesized from equal mixes of the two parent RNAs.
Genotyping:
Genes of interest were PCR amplified from genomic DNAs of the hybrid poplars. The PCR products were sequenced using Big Dye Terminator 3.1 sequencing chemistry (Applied Biosystems, Foster City, CA) by the Nucleic Acids Protein Service (NAPS) unit at the University of British Columbia. Single nucleotide polymorphisms (SNPs) in exon regions were identified and selected for allele-specific expression analysis. Common SNPs were selected for the four hybrid poplars from central British Columbia. The same SNPs were selected for the cis- and trans-regulatory variation analysis if they also existed in the hybrid synthesized by Scott Paper; otherwise other SNPs were selected for this hybrid.
Single-base primer extension assay:
DNA and cDNA segments surrounding the SNPs present in the hybrid poplars were PCR amplified. cDNAs from equally mixed parental RNAs were also PCR amplified. Following PCR thermal cycling, unincorporated primers and dNTPs were removed by adding 1.67 units of shrimp alkaline phosphatase (SAP) (Fermentas, Burlington, Ontario) and 1 unit of Exonuclease I (Fermentas) to each 5-µl PCR product. Reactions were mixed briefly and incubated at 37° for 60 min then 80° for 15 min. The PCR products were then subjected to a primer extension assay (SNaPshot, Applied Biosystems) using extension primers designed to anneal to the amplified DNA adjacent to the SNP site (supplemental Table 2 at http://www.genetics.org/supplemental/). Primer extension reactions were carried out in a total volume of 10 µl containing 0.5 µl ABI Prism SNaPshot multiplex kit mix (Applied Biosystems), 0.2 µM extension primer, 2 µl of PCR product, and 6.5 µl of deionized water. Thermal cycling conditions for extension reactions were carried out with the following program: 2 min at 94°, and 25 cycles consisting of 10 sec at 96°, 5 sec at 50°, and 30 sec at 60°. After cycling, the unincorporated fluorescent ddNTPs (dideoxynucleotide triphosphates) were removed by adding 1 unit of SAP and incubating for 60 min at 37°, followed by 15 min at 65° for enzyme inactivation. The resulting primer extension products were analyzed on an ABI 3730 capillary electrophoresis DNA instrument, using GeneMapper 3.7 software (Applied Biosystems) according to the manufacturer's protocol. The expression percentages of the two alleles were measured by comparing the peak heights. Since differing fluorophores may influence the incorporation and migration rates of four types of ddNTPs, the peak heights are not always identical between two alleles of equal abundance (PINSONNEAULT et al. 2004). Therefore, allelic ratios of genomic DNAs assumed to be present in equal amounts (ratio = 1) were used to normalize allelic ratios of cDNA samples (PINSONNEAULT et al. 2004; WANG et al. 2005). Genes showing expression of only one allele were further examined with direct sequencing of the RT–PCR products to confirm the monoallelic expression patterns.
Statistical analyses:
Standard errors of replicates were calculated. Two-tailed homoscedastic variance t-tests (P = 0.05) were performed with Microsoft Excel to test whether the expression differed between leaves and stems. Two-tailed homoscedastic variance t-tests (P = 0.05) were also used to assess the difference between the allelic expression ratio in the F1 hybrid vs. that in mixed parental RNA compared with a 50:50 value.
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RESULTS |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
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Allele-specific gene expression analysis:
We studied the allelic expression variation for 30 genes in four Populus hybrids using a single base primer extension assay (Figure 1). This method has been shown to be effective in distinguishing between and quantifying sequence variants by a single SNP site (COWLES et al. 2002; NORTON et al. 2002; YAN et al. 2002; BRAY et al. 2003; WANG et al. 2005). Relative expression of the P. trichocarpa derived allele (Pt) for the four hybrids is shown in Table 2. We used 1.5-fold (that is a 60:40 ratio) as a minimum threshold ratio for allelic differential expression because it encompasses the standard error for all genes and represents a conservative estimation of unequal expression. To test the consistency of the expression data among replicates, eight leaf replicates (separate RNA extractions from different leaves) from one of the hybrids were tested for two genes, GT47C and TI5, and the resulting standard errors were 3 and 2%, respectively.
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Organ-specific allelic expression patterns:
We examined leaves and stems to detect organ-specific allelic expression patterns. Expression of 24 genes was assayed in both leaves and stems. Eight genes showed biased allelic expression in the majority of the four hybrids in both leaves and stems, 2 genes only in leaves, and 5 genes only in stems (Table 2). Significant expression differences between leaves and stems were detected for 10 genes when all hybrids and replicates were analyzed together, with a sample size of 8 for each gene in each organ. DXPS showed biased expression in leaves but monoallelic expression in stems; ADK, CaMBP, ISP, PPO3, PPR, and TI5 showed greater allelic expression bias in stems than in leaves; Cel9B and SKOR showed higher bias in leaves than in stems; and MATE showed different parental alleles being preferably expressed between leaves and stems (Figure 2).
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50:50. 50:50, Pd:Pt (hybrid) = 50:50. Pd:Pt (hybrid), Pd:Pt (hybrid) 50:50, Pd:Pt (parent) 50:50. For the 19 genes examined, 6 were classified as cis-regulated, 1 gene as trans-regulated (CaMBP for a calmodulin binding protein), and 9 were considered to be adjusted by combined cis- and trans-regulation (Figure 3, Table 3). Among these 9 genes, 5 showed allelic biases in the same direction and 2 (GT47C and Cel9B) had allelic expression biases in the opposite direction. Three genes (ADH, P4H, and Unknown2) showed equal expression in the parents but biased allelic expression in the hybrid and these genes do not show evidence of either cis- or trans-regulation. Instead those genes show allelic variation in the F1 hybrid (Table 3).
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DISCUSSION |
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10% of genes with >1.5-fold allelic expression difference (COWLES et al. 2002). There appears to be a higher degree of allelic expression variation in the Populus hybrids and the maize hybrids than in the mouse hybrids. It has been suggested that the highly polymorphic maize genome could account for its relatively high degree of allelic expression variation (GUO et al. 2004). Similarly, the genetic divergence between P. trichocarpa and P. deltoides probably contributes to a higher allelic expression variation compared to the mouse intraspecific hybrids.
Organ-specific differences in allelic expression:
We observed allelic expression differences between leaves and stems for 10 of 15 genes (67%) that were expressed in both organs and showed allelic expression variation. Although the sample size is relatively small, the results still suggest a surprisingly high degree of organ-specific differences in allelic expression. It was previously shown in a diploid F1 cotton hybrid that the AdhA gene showed organ-specific allelic silencing (ADAMS and WENDEL 2005). A study done concurrently to the research reported here examined allelic expression in three organs of intraspecific maize hybrids and found that about half of the genes that were expressed in all three organs showed different allelic ratios in at least one of the three organs (SPRINGER and STUPAR 2007b). Similarly, a study of mouse intraspecific hybrids identified two genes with diverged allelic expression patterns in different tissues (COWLES et al. 2002). The above studies have established that allelic expression in hybrids can be highly tissue- and organ-specific. In future studies of individual cell types, it would be interesting to characterize allelic expression at a finer scale.
Gene regulatory variation in hybrids:
The comparison of expression between a mix of parental RNAs and F1 hybrid RNA revealed 6 of 19 (32%) genes under mainly cis-regulation, 1 of 19 (5%) under primarily trans-regulation, and 9 genes (47%) controlled coordinately by cis- and trans-regulation. Therefore cis-regulation, sometimes in combination with trans-regulation, appears to be largely responsible for the regulation of the genes in our study. Studies of interspecific Drosophila hybrids reported 12 of 28 (43%) genes to be completely explained by cis-regulation, and the remaining 16 all explained by cis- and trans-regulation (WITTKOPP et al. 2004). This contrasts to the findings in maize intraspecific hybrids that showed pure cis-regulation accounting for allelic expression in 18 of 35 (51%), a majority of the sampled genes (STUPAR and SPRINGER 2006). Although variable proportions of complete cis-regulation are found in the various studies of different organisms, cis-effects were consistently involved in most if not all of the assayed genes, and pure trans-regulation is rare, affecting only 1 of 19 genes in the Populus hybrids, 1 of 35 in the maize hybrids (STUPAR and SPRINGER 2006), and none of 28 in the Drosophila hybrids (WITTKOPP et al. 2004). Cis- and trans-regulation were explored at a much larger scale in a recently published study of maize hybrids that examined 316 genes and found that pure cis-regulation predominates. As cis-elements function in an allele-specific manner, allelic expression following cis-regulation reflects an inheritance of the regulatory pattern from the two parents to the hybrid.
Hybridization induced changes in allelic expression:
After hybridization both alleles are exposed to common trans-regulators in the same cellular environment, and so trans-regulation and combined cis- and trans-regulation could be induced by hybridization to harmonize the two heterozygous genomes (LANDRY et al. 2005). There is a hypothesis that cis- and trans-compensatory evolution is important in leading to novel gene expression and performance in the hybrids (LANDRY et al. 2005). Compensatory cis- and trans-regulation is inferred when the allelic expression difference in an F1 hybrid is more extreme than, or in the opposite direction from, that in the parents, suggesting changes in trans- compensate for the already existing cis-divergence. In this study 4 of 19 genes display allelic expression biases to a larger extent in the hybrid than in the parents, and 3 other genes, Cel9B, GT47C, and Unknown2 clearly show opposite allelic divergence in the hybrid compared with the parental divergence. It has been proposed that reuniting diverged regulatory factors and hierarchies in hybrids can lead to altered gene expression patterns (RIDDLE and BIRCHLER 2003). The cases involving trans-regulation in Populus hybrids suggest a modification of the regulatory network upon interspecific hybridization that affects expression of some genes.
Three genes in this study (ADH, P4H, and Unknown2) showed equal expression in the parents but biased allelic expression in the F1 hybrid indicating expression variation in the hybrid that could not necessarily be classified as trans-regulation according to the test we used. Other factors, such as epigenetic variation, might account for the expression changes in those genes.
The Populus F1 hybrids used in this study show strong heterosis, particularly in regards to growth rate, trunk diameter, stem diameter, and leaf size. Might altered gene regulation in F1 hybrids observed in this study be involved in generating the heterotic phenotypes observed in these hybrids? Although no data from this study provide evidence for that possibility, it has been proposed that another type of altered gene regulation in F1 hybrids, deviations from mid-parent expression levels, may contribute to heterosis (BIRCHLER et al. 2003; SWANSON-WAGNER et al. 2006). It is tempting to speculate that altered gene regulation in the Populus hybrids, especially monoallelic expression, may play a role in the heterosis seen in this system, although future studies will be needed to test this hypothesis.
Expression changes upon hybridization in diploid hybrids compared with allopolyploid hybrids:
Allopolyploid hybrids can be formed by hybridization between two diploid species followed by spontaneous or induced chromosome doubling. Altered gene expression levels and patterns in an F1 hybrid could be directly passed on to the allopolyploid if there is chromosome doubling in the F1 hybrid. Indeed studies of newly synthesized allopolyploids have revealed considerable alterations in gene expression compared with their parents (COMAI et al. 2000; KASHKUSH et al. 2002; ADAMS et al. 2004; WANG et al. 2004, 2006a; HEGARTY et al. 2005, 2006), much of which have been shown to be caused by interspecific hybridization instead of chromosome doubling. An important distinction between expression changes caused by hybridization in diploid hybrids vs. allopolyploid hybrids is that expression patterns of alleles in diploid hybrids are more likely to experience homogenization in subsequent generations, if there is recombination between the alleles, than homeologous genes in allopolyploids that may maintain distinct expression patterns over evolutionary time if there is no intergenomic recombination.
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ACKNOWLEDGEMENTS |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
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LITERATURE CITED |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
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