Transcriptome analysis of rice root heterosis by RNA-Seq
- Rongrong Zhai†1,
- Yue Feng†1,
- Huimin Wang2,
- Xiaodeng Zhan1,
- Xihong Shen1,
- Weiming Wu1,
- Yingxin Zhang1,
- Daibo Chen1,
- Gaoxing Dai3,
- Zhanlie Yang4,
- Liyong Cao1Email author and
- Shihua Cheng1Email author
© Zhai et al.; licensee BioMed Central Ltd. 2013
Received: 29 June 2012
Accepted: 3 January 2013
Published: 16 January 2013
Heterosis is a phenomenon in which hybrids exhibit superior performance relative to parental phenotypes. In addition to the heterosis of above-ground agronomic traits on which most existing studies have focused, root heterosis is also an indispensable component of heterosis in the entire plant and of major importance to plant breeding. Consequently, systematic investigations of root heterosis, particularly in reproductive-stage rice, are needed. The recent advent of RNA sequencing technology (RNA-Seq) provides an opportunity to conduct in-depth transcript profiling for heterosis studies.
Using the Illumina HiSeq 2000 platform, the root transcriptomes of the super-hybrid rice variety Xieyou 9308 and its parents were analyzed at tillering and heading stages. Approximately 391 million high-quality paired-end reads (100-bp in size) were generated and aligned against the Nipponbare reference genome. We found that 38,872 of 42,081 (92.4%) annotated transcripts were represented by at least one sequence read. A total of 829 and 4186 transcripts that were differentially expressed between the hybrid and its parents (DGHP) were identified at tillering and heading stages, respectively. Out of the DGHP, 66.59% were down-regulated at the tillering stage and 64.41% were up-regulated at the heading stage. At the heading stage, the DGHP were significantly enriched in pathways related to processes such as carbohydrate metabolism and plant hormone signal transduction, with most of the key genes that are involved in the two pathways being up-regulated in the hybrid. Several significant DGHP that could be mapped to quantitative trait loci (QTLs) for yield and root traits are also involved in carbohydrate metabolism and plant hormone signal transduction pathways.
An extensive transcriptome dataset was obtained by RNA-Seq, giving a comprehensive overview of the root transcriptomes at tillering and heading stages in a heterotic rice cross and providing a useful resource for the rice research community. Using comparative transcriptome analysis, we detected DGHP and identified a group of potential candidate transcripts. The changes in the expression of the candidate transcripts may lay a foundation for future studies on molecular mechanisms underlying root heterosis.
KeywordsHeterosis Root Transcriptome RNA-Seq Hybrid rice
Heterosis is a phenomenon in which hybrids exhibit superior phenotypes, such as enhanced biomass production, development rate, grain yield, and stress tolerance, relative to their parents. Heterosis has been effectively utilized to increase crop production in the world. It is estimated, for example, that hybrid rice, which occupies more than 50% of the total rice area in China, has a 10–20% yield advantage over inbred varieties . Our knowledge of the genetic mechanisms of heterosis, however, has lagged behind its wide application. Two hypotheses-dominance [2, 3] and over-dominance [4, 5]-were proposed in the early 20th century to interpret heterosis. Both describe nonadditive behavior as a consequence of genetic differences between distinct homozygous parental lines and their heterozygous hybrids . With the advent of molecular makers, quantitative trait locus (QTL) mapping has become a routine tool for studying the genetic basis of heterosis in crop plants; so far, however, the QTL analysis has not contributed much to the understanding of heterosis.
With the development of functional genomics, the technique of large-scale transcriptome analysis-based on cDNA or expressed sequence tag (EST) library sequencing, microarray hybridization, and serial analysis of gene expression (SAGE)-has been used to investigate heterosis in Arabidopsis[7, 8], maize , and rice [10–12]. Such technologies offer the potential to unveil the molecular basis of heterosis at the transcriptional level [13, 14]. These technologies have drawbacks, however, such as low throughput, high cost, low sensitivity, cloning bias, high background signal, and pre-determined probes requirements . Next-generation high-throughput RNA sequencing technology (RNA-Seq) is a recently-developed method for discovering, profiling, and quantifying RNA transcripts with several advantages over other expression profiling technologies including higher sensitivity and the ability to detect splicing isoforms and somatic mutations . Using RNA-Seq, significant progress has been made in understanding the transcript expression of rice over the last two years [15, 17–21]. For example, transcriptome analysis of rice mature root tissue and root tips at two time points identified 1761 root-enriched transcripts and 306 tip-enriched transcripts involved in different physiological processes . In addition, RNA-Seq has been applied to the identification of stress-inducible transcripts in rice [17, 21]. Other than a transcriptome analysis of seedling shoots at the four-leaf stage , however, little effort is being expended in attempts to investigate heterosis using RNA-Seq.
Plant root systems serve a number of important functions, including anchoring the plant, absorbing water and nutrients, producing amino acids and hormones, and secreting organic acids, enzymes, and alkaloids. In recent years, considerable research and interest has focused on root systems. Some of these studies have demonstrated that heterosis levels might be higher in root traits than in aboveground agronomic traits [22–24], which suggests that roots might be an ideal organ for investigating the genetic basis of rice heterosis. Several attempts have been made to discover the molecular mechanism of root heterosis at the vegetative stage [25–27], but little attention has been paid to heterosis in the root system during the late growth stage, when accumulation, transportation, and distribution of dry matter, and ultimately, yield potential, may be influenced. There has currently been no systematic investigation into root heterosis at the two different developmental stages.
In this study, we focused our heterosis research on the late-stage high-vigor super-hybrid rice variety, Xieyou 9308, which has a grain yield of up to 12.23 × 103 kg • hm-2 and was designated as “super rice” by the Chinese Ministry of Agriculture in 2005. Xieyou 9308 was bred by crossing the restorer line R9308 (with 25% japonica genetic components) to the maternal line Xieqingzao B (indica). We used RNA-Seq to investigate the global transcriptomes of roots from Xieyou 9308 and its parents at tillering and heading stages. Differentially expressed transcripts and their expression patterns were analyzed, and several potential candidate transcripts were found to be involved in carbohydrate metabolism and plant hormone signal transduction pathways. We expect this genome-wide transcriptome comparison to provide a starting point to understand the causative mechanism of the altered gene expression in the hybrid and the molecular mechanism underlying rice root heterosis.
Characterization of Xieyou 9308 and its two parental lines
Mid-parent heterosis and high-parent heterosis of root traits at tillering and heading stages
Root length (cm)
Root dry weight (g)
Shoot dry weight (g)
Root length (cm)
Root dry weight (g)
Shoot dry weight (g)
Mapping reads to the rice genome
Number of mapped reads
Total filtered reads
Transcriptome profiles of Xieyou 9308 and its parents
Identification of differentially expressed genes (DEGs) by RNA-Seq
Number and classification of DEGs
Functional classification by Gene Ontology (GO)
Significant GO terms of DG HP in the biological process category at the tillering stage
carbohydrate metabolic process
photosynthesis, light harvesting
response to oxidative stress
chitin catabolic process
cell wall macromolecule catabolic process
glucose metabolic process
regulation of nitrogen utilization
response to biotic stimulus
electron transport chain
terpenoid biosynthetic process
defense response to fungus
L-methionine salvage from methylthioadenosine
chlorophyll biosynthetic process
defense response to bacterium
The top 20 most represented GO terms of DG HP in the biological process category at the heading stage
regulation of transcription
carbohydrate metabolic process
response to oxidative stress
cellulose biosynthetic process
cellular metabolic process
photosynthesis, light harvesting
recognition of pollen
drug transmembrane transport
Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway mapping
The above DGHP were then classified into 164 subcategories that corresponded to their functions. We further identified KEGG Orthology (KO) terms that were over-represented in the DGHP (Additional file 6: Table S3 and Additional file 6: Table S4). Carbon fixation, photosynthesis, photosynthesis-antenna protein pathways, and fructose and mannose metabolism were over-represented at both stages. In contrast, KO terms related to signal transduction, glycolysis/gluconeogenesis, amino sugar and nucleotide sugar metabolism, and starch and sucrose metabolism were highly enriched in DGHP and were exclusively expressed at the heading stage (Additional file 7: Figure S4). This suggests that there are considerable differences in root physiological processes between the tillering stage and the heading stage. These annotations provide a valuable resource for investigating specific processes, functions, and pathways underlying heterosis.
Validation by quantitative real-time PCR (qRT-PCR)
Although heterosis has been widely exploited in plant breeding and plays an important role in agriculture, the molecular and genetic mechanisms underlying the phenomenon remain poorly understood. Differential gene expression between a hybrid and its parents may be associated with heterosis [10–12, 18, 31]. In this study, we used RNA-Seq to investigate the relationship between transcriptional profiles and heterosis in a super-hybrid rice combination, Xieyou 9308. In our RNA-Seq analysis, 391 million high-quality 100-bp paired-end reads were generated from the roots of Xieyou 9308 and its parental lines at tillering and heading stages, and 38,872 annotated transcripts were identified. On average, 9301 reads were detected per identified annotated transcript, providing approximately 70-fold coverage of the transcriptome. From the annotated transcripts, 829 DGHP at the tillering stage and 4186 DGHP at the heading stage were identified. These results suggest that the expression of DGHP at the heading stage may play a more important role in root heterosis than that at the tillering stage. Additionally, only a small fraction of transcripts may be responsible for root heterosis at the transcriptional level in Xieyou 9308.
Comparative analysis of annotated DGHP
Comparative transcriptome analysis revealed a subset of transcripts that were differently expressed between the hybrid and its parents at tillering and heading stages. Some potential regulators for heterosis in root development were uncovered. At the tillering stage, a large number of DGHP related to carbon fixation in photosynthetic organisms, photosynthesis, and photosynthesis-antenna proteins were found. Transcripts involved in plant hormone signal transduction, carbon fixation in photosynthetic organisms, photosynthesis, photosynthesis-antenna proteins, and carbohydrate metabolism (including glycolysis and starch/sucrose, fructose/mannose, glucose/galactose, and pyruvate metabolism) were highly expressed in roots at the heading stage. We therefore conclude that carbohydrate metabolism and plant hormone signal transduction pathways may contribute significantly to root development. Another result of interest is the differential expression of photosynthetic transcripts at both stages. The observed gene expression may be related to culture effects because the expression of these transcripts is not generally observed in roots of soil-grown plants . In our study, plants were cultured under hydroponic conditions; the roots may have thus been passively exposed to light, which could strongly activate photosynthesis in root tissues. A similar result was observed in another recent study, along with the finding that a large number of DEGs were involved in photosynthesis in roots . In this study, we found that most of the DGHP were down-regulated at the tillering stage and up-regulated at the heading stage. Because Xieyou 9308 is a late-stage high-vigor super-hybrid rice variety, root heterosis might be expected to be stronger at the heading stage than at the tillering stage. For these reasons, subsequent analyses that focus on the expression of DGHP at the heading stage are warranted.
The role of carbohydrate metabolism in heterosis
Some enzymes involved in glycolysis pathways, such as phosphofructose kinase (PFK), fructose-bisphosphate aldolase (FBA), glyceraldehyde-3-phosphate dehydrogenase (GAPDH), phosphoglycerate kinase (PGK), pyruvate kinase (PK), alcohol dehydrogenase (ADH), pyruvate decarboxylase (PDC), and lactate dehydrogenase (LDH), were up-regulated in Xieyou 9308. The reaction catalyzed by PFK is the rate-limiting step of glycolysis; up-regulated PFK (Os05t0524400) may therefore reduce the limitation. In addition, three DGHP (Os07t0181000, Os11t0148500, and Os12t0145700) that encode PK were up-regulated in Xieyou 9308. Interestingly, the expression of OsPK1 (Os11t0148500) is stronger in adventitious roots than in the primary root, both of which serve as execution sites of absorption . This suggests that Xieyou 9308 may have a stronger absorption capacity than its parental lines. Transcriptional expression levels of FBA (Os05t0402700, Os08t0120600, and Os11t0171300), which plays an important physiological role in accelerating cell growth and promoting root elongation , were up-regulated. In addition, transcriptional expression levels of LDH (Os02t0105400 and Os06t0104900), PDC (Os03t0293500, Os05t0469600, Os05t0469800, Os09t0371500, and Os10t0480900), and ADH (Os11t0210300, Os11t0210500, and Os11t0210600), which are involved in glycolysis pathways, were up-regulated. It has been suggested that the lactate initially produced by LDH lowers the pH, which in turn activates PDC and ADH [43, 44]. LDH, PDC, and ADH transcripts may be involved in inducing the hypoxia pathway; their up-regulation in this study may be due to the anaerobic stress that the roots might have experienced in the hydroponic solution [45–47].
In contrast to animal cells, plant cells are enclosed by cell walls, which not only determine cell shape and provide structural support but also protect the plant against environmental stresses and regulate plant growth [48, 49]. Cellulose is the most abundant biopolymer and the main structural component of plant cell walls. Our transcriptional profile analysis identified up-regulated transcripts that were related to cellulose synthesis, including cellulose synthase (CesA) (Os01t0750300, Os03t0808100, Os03t0837100, Os05t0176100, Os07t0208500, Os07t0208533, Os07t0252400, Os07t0424400, Os09t0422500, and Os10t0467800) and β-1, 4-endoglucanase (EGase) (Os03t0736300 and Os04t0497200). CesA up-regulation can promote root hair elongation, thus improving the absorption of water and nutrients by roots [50, 51]. Interestingly, a previous study found that high expression of OsGLU3 (Os04t0497200) can affect root cell wall cellulose synthesis and thus modulate root elongation and protect roots from environmental stresses .
Complex regulation of plant hormone signal transduction
In multicellular organisms, cellular communication is important for coordinating the growth and differentiation of cells into new tissues and organs. As is well known, hormones act as signaling molecules in plants by mediating physiological responses. Similar to the results in studies by Kyndt et al. and Wang et al., our transcriptome analysis uncovered many DGHP that were involved in the phytohormone response in root tissues. To illustrate, the abscisic acid (ABA) pathway is involved in the repression of lateral root development and adaption to environmental stresses [53, 54]. In our study, many ABA-responsive transcripts exhibited different expression levels between the hybrid and its parents. For example, mRNA levels of four transcripts (Os03t0610900, Os04t0432000, Os07t0622000, and Os12t0586100) encoding SNF1-related protein kinase 2 (SnRK2), whose autophosphorylation is required for kinase activity towards downstream targets, were significantly more highly expressed in Xieyou 9308 than in its parents. In addition, similar to previous studies by Cohen et al. and Santiago et al., PYR/PYL ABA receptors (Os02t0255500 and Os10t0573400) were down-regulated, and type-2C protein phosphatase (PP2C, a negative regulator) (Os01t0583100 and Os05t0457200) was up-regulated. These results fit into the negative-feedback regulatory mechanism. Such re-setting of the ABA signaling pathway provides Xieyou 9308 with a dynamic mechanism for monitoring ABA levels and modulating ABA response .
Transcripts involved in the cytokinin (CTK) signaling pathway were also differentially expressed between the hybrid and its two parents in our study. The CTK pathway is involved in two aspects of root growth inhibition: the impedance of primary root elongation and the regulation of lateral root initiation . A subset of CTK-responsive transcripts such as type-A response regulators (RRs-A) (Os01t0952500, Os02t0557800, Os04t0442300, and Os12t0139400) and type-B response regulators (RRs-B) (Os02t0796500, Os03t0224200, and Os06t0183100), showed significantly different expression patterns in root tissues. RRs-B are positive transcriptional regulators in the CTK signaling pathway, whereas RRs-A act as negative regulators . The most likely model for this interaction is one in which RRs-A inhibit the activation of RRs-B by competing for phosphotransfer from upstream histidine phosphotransfer proteins; this model has been demonstrated in a few bacterial two-component systems [60–62]. Furthermore, previous studies have demonstrated that root elongation and lateral root formation in type-A mutants is more sensitive to CTK inhibition, and type-B mutants exhibit the opposite behavior [63–65]. The up-regulated RRs-A and down-regulated RRs-B observed in our study may thus work together to lessen the sensitivity of Xieyou 9308 root tissues to CTK inhibition.
Comparison of significant DGHPwith QTLs for yield and root traits
Significant differentially expressed transcripts located in each of the QTL regions
RL, TRL, RSA, RV, RTN, RDW
GYD, NP, NSP, HD
In hybrids, diversity in gene expression can be the result of variation in cis-regulatory elements (e.g., promoter regions) or trans-regulatory elements (e.g., transcription factors) . If differential expression of a gene is cis-induced, the gene may be located in a QTL region, whereas if it is trans-induced, a QTL may correspond with the trans-regulatory elements and be located distantly from the gene locus. In our DGHP collections, we indeed found that some DGHP encoded transcription factors, which may be involved in trans-regulation, in the QTL regions (Additional file 9: Table S6). The expression of candidate transcripts in these QTL regions may serve as a starting point to understand the molecular mechanisms underlying heterosis. The application of these results is expected to provide an opportunity to breed elite rice varieties that process both yield and root heterosis.
In this study, we used RNA-Seq to systematically investigate the global transcriptomes of roots from the super-hybrid rice Xieyou 9308 and its parents at tillering and heading stages, generating a useful resource for the rice community. We analyzed DGHP and compared them with QTLs for yield and root traits, providing clues for candidate transcripts that may significantly contribute to root development and yield production. The changes in the expression of candidate transcripts may provide valuable information for future studies on molecular mechanisms underlying root heterosis.
Plant materials and growing conditions
Xieyou 9308, a super-hybrid rice variety commonly planted in China, and its parents Xieqingzao B (female) and R9308 (male) were used in this study. All experiments were conducted in 2011. Rice seeds were surface-sterilized with 3% H2O2 for 10 min and then rinsed several times with distilled water. After soaking in distilled water at 37°C for 2 d, germinated seeds were sown in the field at the China National Rice Research Institute, Fuyang, China. After approximately 30 d, 40 seedlings of each genotype were transplanted into plots of plastic foam floating in a pool filled with nutrient solution. Roots were sampled with ten replicates at tillering and heading stages to measure root traits and estimate heterosis. In addition, two roots of every genotype at each stage were collected and stored at −80°C in preparation for RNA-Seq analysis.
Root heterosis measurements
To determine dry weight and root-shoot ratio, shoots and root systems were placed in an oven set at 110°C for 80 min, followed by drying at 80°C for 4 d. Root length was measured manually. MPH and HPH were calculated according to the following formulas: MPH = (F1 − MP)/MP in % and HPH = (F1 − HP)/HP in %, where F1 is the performance of the hybrid, MP is the average performance of the two parents, and HP is the best performance of the two parents. Hypothesis testing was performed using t-test.
RNA extraction, cDNA library preparation, and sequencing
Total RNA was extracted from roots using Trizol reagent (Invitrogen, Carlsbad, CA, USA) and purified using RNeasy Plant Mini Kit (Qiagen, Valencia, CA). The RNA quality was checked on a Bioanalyzer 2100 (Aligent, Santa Clara, CA); RNA Integrity Number (RIN) values were greater than 8.5 for all samples. Sequencing libraries were prepared according to the manufacturer’s instructions (Illumina, San Diego, CA). Poly-A-containing mRNA was isolated from the total RNA, subjected to two purification rounds using poly-T oligo-attached magnetic beads, and fragmented using an RNA fragmentation kit. First strand cDNA was generated using reverse transcriptase and random primers. Following the second strand cDNA synthesis and adaptor ligation, 200-bp cDNA fragments were isolated using gel electrophoresis and amplified by 18 cycles of PCR. The products were loaded onto an Illumina HiSeq2000 instrument and subjected to 100 cycles of paired-end (2 × 100 bp) sequencing. The processing of fluorescent images into sequences, base-calling and quality value calculations were performed using the Illumina data processing pipeline (version 1.8). The sequence reads were submitted to GenBank GEO database under accession number GSE41797 (http://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE41797).
Mapping of short reads and assessment of differential gene expression
Raw reads were filtered to obtain high-quality reads by removing low-quality reads containing more than 30% bases with Q < 20. After trimming low-quality bases (Q < 20) from the 5' and 3' ends of the remaining reads, the resulting high-quality reads were mapped onto the Nipponbare reference genome (IRGSP build 5.0) using RSEM (v1.1.11) . Differential expression was estimated and tested with the software package edgeR (R version: 2.14, edgeR version: 2.3.52) ; we quantified gene expression levels in terms of RPKM , calculated FDR, and estimated FC and log2 values of FC. Transcripts that exhibited an FDR ≤ 0.05 and an estimated absolute log2 (FC) ≥ 1 were determined to be significantly differentially expressed. The transcript coverage was calculated as the number of mapped reads in a locus multiplied by 100 bp and then divided by the summed exon length of the locus.
For statistical analysis, we used the following analysis of variance (ANOVA) model: y = u + (GA) + (GD) + (SR) + e, where y is the acquired gene expression, u is the overall mean, GA is the additive effect, GD is the dominant effect, SR is the replication effect, and e is the residual error. The d/a ratio, also referred to as dominance ratio or potence, hp (where a and d represent GA and GD, respectively [77, 78]), was calculated to measure the nonadditivity of the F1 hybrid relative to the parents. To avoid troublesome statistical properties, Vuylsteke et al. proposed using d - a (d > 0) or d + a (d < 0) instead of d/a. We accordingly constructed 99.8% confidence intervals for d - a (d > 0) and d + a (d < 0). If d > 0 and the confidence interval constructed for d - a included zero, then hp = 1. When the confidence interval did not include zero and was positive, then hp > 1. An analogous procedure was applied for d + a (d < 0).
Cluster analysis was carried out for all annotated transcripts from the hybrid Xieyou 9308 and its parents at tillering and heading stages. The RPKM-normalized expression counts for each transcript were clustered with the software Cluster 3.0, and the results were visualized using Treeview .
Validation of RNA-Seq by qRT-PCR
Total RNA from two sequenced samples and two new samples was treated with DNase, and first-strand cDNA was generated using a RevertAid First Strand cDNA Synthesis kit (Fermentas, Vilnius, Lithuania). SYBR-based qRT-PCR reactions (SYBR Green I, Osaka, Japan) were performed on a LightCycler 480 system (Roche, Basel, Switzerland) using the following reaction conditions: 95°C for 1 min followed by 40 cycles of 95°C for 10 s and 60°C for 30 s. All qRT-PCR reactions were performed in triplicate, and the results were analyzed with the system’s relative quantification software (ver.1.5) based on the delta-delta-Ct method (Roche). The detection threshold cycle for each reaction was normalized against the expression level of the rice Actin1 gene with primer sequences 5'-TGGCATCTCTCAGCACATTCC-3' and 5'-TGCACAATGGATGGGTCAGA-3'.
Differentially expressed genes
Differentially expressed genes between the hybrid and its parents
Quantitative trait locus
Expressed sequence tag
Serial analysis of gene expression
RNA sequencing technology
Web Gene Ontology Annotation Plot
Kyoto Encyclopedia of Genes and Genomes
Quantitative real-time PCR
Rice Annotation Project Database
SNF1-related protein kinase 2
Type-2C protein phosphatase
Type-A response regulators
Type-B response regulators
Root dry weight
Total root length
Root surface area
Root tip number
Root average diameter
Grain yield per plant
Number of panicles
Number of spikelets per panicle
This work was supported by a grant from the Chinese Natural Science Foundation (31071398) and a grant from the National Program on Super Rice Breeding, Ministry of Agriculture. We thank Q Zhao for technical support and excellent discussions, and the associate editor and two anonymous reviewers for their valuable suggestions.
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