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.
- Cheng SH, Zhuang JY, Fan YY, Du JH, Cao LY: Progress in research and development on hybrid rice: a super-domesticate in China. Ann Bot. 2007, 100: 959-966. 10.1093/aob/mcm121.PubMed CentralView ArticlePubMed
- Davenport CB: Degeneration, albinism and inbreeding. Science. 1908, 28: 454-View ArticlePubMed
- Bruce AB: The mendelian theory of heredity and the augmentation of vigor. Science. 1910, 32: 627-628.View ArticlePubMed
- East EM: Inbreeding in corn. Rep Connecticut Agric Exp Stn 1907. 1908, 419-428.
- Shull GH: The composition of a field of maize. Am Breed Assoc Rep. 1908, 4: 296-301.
- Hochholdinger F, Hoecker N: Towards the molecular basis of heterosis. Trends Plant Sci. 2007, 12: 427-432. 10.1016/j.tplants.2007.08.005.View ArticlePubMed
- Wang J, Tian L, Lee HS, Wei NE, Jiang H, Watson B, Madlung A, Osborn TC, Doerge R, Comai L, et al: Genomewide nonadditive gene regulation in Arabidopsis allotetraploids. Genetics. 2006, 172: 507-517.PubMed CentralView ArticlePubMed
- Fujimoto R, Taylor JM, Shirasawa S, Peacock WJ, Dennis ES: Heterosis of Arabidopsis hybrids between C24 and Col is assiciated with increased photosynthesis capacity. Proc Natl Acad Sci. 2012, 109: 7109-7114. 10.1073/pnas.1204464109.PubMed CentralView ArticlePubMed
- Thiemann A, Fu J, Schrag TA, Melchinger AE, Frisch M, Scholten S: Correlation between parental transcriptome and field data for the characterization of heterosis in Zea mays L. Theor Appl Genet. 2010, 120: 401-413. 10.1007/s00122-009-1189-9.View ArticlePubMed
- Ge X, Chen W, Song S, Wang W, Hu S, Yu J: Transcriptomic profiling of mature embryo from an elite super-hybrid rice LYP9 and its parental lines. BMC Plant Biol. 2008, 8: 114-10.1186/1471-2229-8-114.PubMed CentralView ArticlePubMed
- Song GS, Zhai HL, Peng YG, Zhang L, Wei G, Chen XY, Xiao YG, Wang L, Chen YJ, Wu B, et al: Comparative transcriptional profiling and preliminary study on heterosis mechanism of super-hybrid rice. Mol Plant. 2010, 3: 1012-1025. 10.1093/mp/ssq046.PubMed CentralView ArticlePubMed
- Wei G, Tao Y, Liu G, Chen C, Luo R, Xia H, Gan Q, Zeng H, Lu Z, Han Y, et al: A transcriptomic analysis of superhybrid rice LYP9 and its parents. Proc Natl Acad Sci. 2009, 106: 7695-7701. 10.1073/pnas.0902340106.PubMed CentralView ArticlePubMed
- Tirosh I: A yeast hybrid provides insight into the evolutiona of gene expression regulation. Science. 2009, 324: 659-662. 10.1126/science.1169766.View ArticlePubMed
- Zhang X, Borevitz JO: Global analysis of allele-specific expression in Arabidopsis thaliana. Genetics. 2009, 182: 943-954. 10.1534/genetics.109.103499.PubMed CentralView ArticlePubMed
- Kyndt T, Denil S, Haegeman A, Trooskens G, De Meyer T, Van Criekinge W, Gheysen G: Transcriptome analysis of rice mature root tissue and root tips in early development by massive parallel sequencing. J Exp Bot. 2012, 63: 2141-2157. 10.1093/jxb/err435.View ArticlePubMed
- Wang Z, Gerstein M, Snyder M: RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet. 2009, 10: 57-63. 10.1038/nrg2484.PubMed CentralView ArticlePubMed
- Oono Y, Kawahara Y, Kanamori H, Mizuno H, Yamagata H, Yamamoto M, Hosokawa S, Ikawa H, Akahane I, Zhu Z, et al: mRNA-Seq reveals a comprehensive transcriptome profile of rice under phosphate stress. Rice. 2011, 4: 50-65. 10.1007/s12284-011-9064-0.View Article
- He G, Zhu X, Elling AA, Chen L, Wang X, Guo L, Liang M, He H, Zhang H, Chen F, et al: Global epigenetic and transcriptional trends among two rice subspecies and their reciprocal hybrids. Plant Cell. 2010, 22: 17-33. 10.1105/tpc.109.072041.PubMed CentralView ArticlePubMed
- Lu T, Lu G, Fan D, Zhu C, Li W, Zhao Q, Feng Q, Zhao Y, Guo Y, Huang X, et al: Function annotation of the rice transcriptome at single-nucleotide resolution by RNA-seq. Genome Res. 2010, 20: 1238-1249. 10.1101/gr.106120.110.PubMed CentralView ArticlePubMed
- Zhang G, Guo G, Hu X, Zhang Y, Li Q, Li R, Zhuang R, Lu Z, He Z, Fang X, et al: Deep RNA sequencing at single base-pair resolution reveals high complexity of the rice transcriptome. Genome Res. 2010, 20: 646-654. 10.1101/gr.100677.109.PubMed CentralView ArticlePubMed
- Mizuno H, Kawahara Y, Sakai H, Kanamori H, Wakimoto H, Yamagata H, Oono Y, Wu J, Ikawa H, Itoh T, Matsumoto T: Massive parallel sequencing of mRNA in identification of unannotated salinity stress-inducible transcripts in rice (Oryza sativa L.). BMC Genomics. 2010, 11: 683-10.1186/1471-2164-11-683.PubMed CentralView ArticlePubMed
- Hoecker N, Keller B, Piepho HP, Hochholdinger F: Manifestation of heterosis during early maize (Zea mays L.) root development. Theor Appl Genet. 2005, 112: 421-429.View ArticlePubMed
- Meyer RC: Heterosis of biomass production in Arabidopsis. Establishment during early development. Plant Physiol. 2004, 134: 1813-1823. 10.1104/pp.103.033001.PubMed CentralView ArticlePubMed
- Bao JY, Lee S, Chen C, Zhang XQ, Zhang Y, Liu SQ, Clark T, Wang J, Cao ML, Yang HM: Serial analysis of gene expression study of a hybrid rice strain (LYP9) and its parental cultivars. Plant Physiol. 2005, 138: 1216-1231. 10.1104/pp.105.060988.PubMed CentralView ArticlePubMed
- Wang Z, Ni Z, Wu H, Nie X, Sun Q: Heterosis in root development and differential gene expression between hybrids and their parental inbreds in wheat (Triticum aestivum L.). Theor Appl Genet. 2006, 113: 1283-1294. 10.1007/s00122-006-0382-3.View ArticlePubMed
- Yao Y, Ni Z, Zhang Y, Chen Y, Ding Y, Han Z, Liu Z, Sun Q: Identification of differentially expressed genes in leaf and root between wheat hybrid and its parental inbreds using PCR-based cDNA subtraction. Plant Mol Biol. 2005, 58: 367-384. 10.1007/s11103-005-5102-x.View ArticlePubMed
- Paschold A, Marcon C, Hoecker N, Hochholdinger F: Molecular dissection of heterosis manifestation during early maize root development. Theor Appl Genet. 2009, 120: 383-388.View Article
- Cheng SH, Cao LY, Zhuang JY, Chen SG, Zhan XD, Fan YY, Zhu DF, Min SK: Super hybrid rice breeding in China:achievements and prospects. J Integr Plant Biol. 2007, 49: 805-810. 10.1111/j.1744-7909.2007.00514.x.View Article
- Pickett AA: Hybrid wheat: results and problems. Adv Plant Breed, Suppl J Plant Breed. 1993, 15: 1-259.
- Ye J, Fang L, Zheng H, Zhang Y, Chen J, Zhang Z, Wang J, Li S, Li R, Bolund L, et al: WEGO: a web tool for plotting GO annotations. Nucleic Acids Res. 2006, 34: 293-297. 10.1093/nar/gkl031.View Article
- Zhang HY, He H, Chen LB, Li L, Liang MZ, Wang XF, Liu XG, He GM, Chen RS, Ma LG, et al: A genome-wide transcription analysis reveals a close correlation of promoter INDEL polymorphism and heterotic gene expression in rice hybrids. Mol Plant. 2008, 1: 720-731. 10.1093/mp/ssn022.View ArticlePubMed
- Wang D, Pan Y, Zhao X, Zhu L, Fu B, Li Z: Genome-wide temporal-spatial gene expression profiling of drought responsiveness in rice. BMC Genomics. 2011, 12: 149-10.1186/1471-2164-12-149.PubMed CentralView ArticlePubMed
- Jackson MB: New Root Formation in Plants and Cuttings. 1986, Martinus Nijhoff Press, NetherlandView Article
- Sharp RE, Silk WK, Hsiao TC: Growth of the maize primary root at low water potentials: I. Spatial distribution of expansive growth. Plant Physiol. 1988, 87: 50-57. 10.1104/pp.87.1.50.PubMed CentralView ArticlePubMed
- Rodriguez HG, Roberts JKM, Jordan WR, Drew MC: Growth, water relations, and accumulation of organic and inorganic solutes in roots of maize seedlings during salt stress. Plant Physiol. 1997, 113: 881-893.PubMed CentralPubMed
- Ogawa A, Yamauchi A: Root osmotic adjustment under osmotic stress in maize seedlings. 2. Mode of accumulation of several solutes for osmotic adjustment in the root. Plant Prod Sci. 2006, 9: 39-46. 10.1626/pps.9.39.View Article
- Jiang K, Zhang S, Lee S, Tsai G, Kim K, Huang H, Chilcott C, Zhu T, Feldman LJ: Transcription profile analyses identify genes and pathways central to root cap functions in maize. Plant Mol Biol. 2006, 60: 343-363. 10.1007/s11103-005-4209-4.View ArticlePubMed
- Ogawa A, Ando F, Toyofuku K, Kawashima C: Sucrose metabolism for the development of seminal root in maize seedlings. Plant Prod Sci. 2009, 12: 9-16. 10.1626/pps.12.9.View Article
- Cho JI, Kim HB, Kim CY, Hahn TR, Jeon JS: Identification and characterization of the duplicate rice sucrose synthase genes OsSUS5 and OsSUS7 which are associated with the plasma membrane. Mol Cells. 2011, 31: 553-561. 10.1007/s10059-011-1038-y.PubMed CentralView ArticlePubMed
- Hirose T, Scofield GN, Terao T: An expression analysis profile for the entire sucrose synthase gene family in rice. Plant Sci. 2008, 174: 534-543. 10.1016/j.plantsci.2008.02.009.View Article
- Zhang Y, Xiao W, Luo L, Pang J, Rong W, He C: Downregulation of OsPK1, a cytosolic pyruvate kinase, by T-DNA insertion causes dwarfism and panicle enclosure in rice. Planta. 2011, 235: 25-38.View ArticlePubMed
- Konishi H, Yamane H, Maeshima M, Komatsu S: Characterization of fructose-bisphosphate aldolase regulated by gibberellin in roots of rice seedling. Plant Mol Biol. 2004, 56: 839-848. 10.1007/s11103-004-5920-2.View ArticlePubMed
- O’Carra P, Mulcahy P: Lactate dehydrogenase in plants: distribution and function. Phytochemistry. 1996, 42: 581-587. 10.1016/0031-9422(95)00978-7.View Article
- Menegus F, Cattaruzza L, Chersi A, Fronza G: Differences in the anaerobic lactate-succinate production and in the changes of cell sap pH for plants with high and low resistance to anoxia. Plant Physiol. 1989, 90: 29-32. 10.1104/pp.90.1.29.PubMed CentralView ArticlePubMed
- Hoffman NE, Bent AF, Hanson AD: Induction of lactate dehydrogenase isozymes by oxygen deficit in barley root tissue. Plant Physiol. 1986, 82: 658-663. 10.1104/pp.82.3.658.PubMed CentralView ArticlePubMed
- Dolferus R, Ellis M, De Bruxelles G, Trevaskis B, Hoeren F, Dennis E, Peacock W: Strategies of gene action in Arabidopsis during hypoxia. Ann Bot. 1997, 79: 21-31. 10.1093/oxfordjournals.aob.a010302.View Article
- Laszlo A, St. Lawrence P: Parallel induction and synthesis of PDC and ADH in anoxic maize roots. Mol Gen Genet. 1983, 192: 110-117. 10.1007/BF00327655.View Article
- Farrokhi N, Burton RA, Brownfield L, Hrmova M, Wilson SM, Bacic A, Fincher GB: Plant cell wall biosynthesis: genetic, biochemical and functional genomics approaches to the identification of key genes. Plant Biotechnol J. 2006, 4: 145-167. 10.1111/j.1467-7652.2005.00169.x.View ArticlePubMed
- Somerville C, Bauer S, Brininstool G, Facette M, Hamann T, Milne J, Osborne E, Paredez A, Persson S, Raab T: Toward a systems approach to understanding plant cell walls. Science. 2004, 306: 2206-2211. 10.1126/science.1102765.View ArticlePubMed
- Kim CM, Park SH, Je BI, Park SJ, Piao HL, Eun MY, Dolan L, Han C: OsCSLD1, a cellulose synthase-like D1 gene, is required for root hair morphogenesis in rice. Plant Physiol. 2007, 143: 1220-1230. 10.1104/pp.106.091546.PubMed CentralView ArticlePubMed
- Wang X, Cnops G, Vanderhaeghen R, De Block S, Van Montagu M, Van Lijsebettens M: AtCSLD3, a cellulose synthase-like gene important for root hair growth in Arabidopsis. Plant Physiol. 2001, 126: 575-586. 10.1104/pp.126.2.575.PubMed CentralView ArticlePubMed
- Zhang JW, Xu L, Wu YR, Chen XA, Liu Y, Zhu SH, Ding WN, Wu P, Yi KK: OsGLU3, a putative membrane-bound endo-1,4-beta-glucanase, is required for root cell elongation and division in rice (Oryza sativa L.). Mol Plant. 2012, 5: 176-186. 10.1093/mp/ssr084.View ArticlePubMed
- Guo D, Liang J, Li L: Abscisic acid (ABA) inhibition of lateral root formation involves endogenous ABA biosynthesis in Arachis hypogaea L. Plant Growth Regul. 2009, 58: 173-179. 10.1007/s10725-009-9365-0.View Article
- De Smet I, Signora L, Beeckman T, Inzé D, Foyer CH, Zhang H: An abscisic acid-sensitive checkpoint in lateral root development of Arabidopsis. Plant J. 2003, 33: 543-555. 10.1046/j.1365-313X.2003.01652.x.View ArticlePubMed
- Cohen D, Bogeat-Triboulot MB, Tisserant E, Balzergue S, Martin-Magniette ML, Lelandais G, Ningre N, Renou JP, Tamby JP, Thiec DL, et al: Comparative transcriptomics of drought responses in Populus: a meta-analysis of genome-wide expression profiling in mature leaves and root apices across two genotypes. BMC Genomics. 2010, 11: 630-10.1186/1471-2164-11-630.PubMed CentralView ArticlePubMed
- Santiago J, Dupeux F, Round A, Antoni R, Park SY, Jamin M, Cutler SR, Rodriguez PL, Márquez JA: The abscisic acid receptor PYR1 in complex with abscisic acid. Nature. 2009, 462: 665-668. 10.1038/nature08591.View ArticlePubMed
- Santiago J, Rodrigues A, Saez A, Rubio S, Antoni R, Dupeux F, Park SY, Márquez JA, Cutler SR, Rodriguez PL: Modulation of drought resistance by the abscisic acid receptor PYL5 through inhibition of clade A PP2Cs. Plant J. 2009, 60: 575-588. 10.1111/j.1365-313X.2009.03981.x.View ArticlePubMed
- Li X, Mo X, Shou H, Wu P: Cytokinin-mediated cell cycling arrest of pericycle founder cells in lateral root initiation of Arabidopsis. Plant Cell Physiol. 2006, 47: 1112-1123. 10.1093/pcp/pcj082.View ArticlePubMed
- Lee DJ, Kim S, Ha YM, Kim J: Phosphorylation of Arabidopsis response regulator 7 (ARR7) at the putative phospho-accepting site is required for ARR7 to act as a negative regulator of cytokinin signaling. Planta. 2007, 227: 577-587.View ArticlePubMed
- Rabin R, Stewart V: Dual response regulators (NarL and NarP) interact with dual sensors (NarX and NarQ) to control nitrate-and nitrite-regulated gene expression in Escherichia coli K-12. J Bacteriol. 1993, 175: 3259-3268.PubMed CentralPubMed
- Li J, Swanson RV, Simon MI, Weis RM: The response regulators CheB and CheY exhibit competitive binding to the kinase CheA. Biochemistry. 1995, 34: 14626-14636. 10.1021/bi00045a003.View ArticlePubMed
- Sourjik V, Schmitt R: Phosphotransfer between CheA, CheY1, and CheY2 in the chemotaxis signal transduction chain of Rhizobium meliloti. Biochemistry. 1998, 37: 2327-2335. 10.1021/bi972330a.View ArticlePubMed
- To JPC, Deruere J, Maxwell BB, Morris VF, Hutchison CE, Ferreira FJ, Schaller GE, Kieber JJ: Cytokinin regulates type-A Arabidopsis response regulator activity and protein stability via two-component phosphorelay. Plant Cell. 2007, 19: 3901-3914. 10.1105/tpc.107.052662.PubMed CentralView ArticlePubMed
- Mason MG: Multiple type-B response regulators mediate cytokinin signal transduction in Arabidopsis. Plant Cell. 2005, 17: 3007-3018. 10.1105/tpc.105.035451.PubMed CentralView ArticlePubMed
- Tsai YC, Weir NR, Hill K, Zhang W, Kim HJ, Shiu SH, Schaller GE, Kieber JJ: Characterization of genes involved in cytokinin signaling and metabolism from rice. Plant Physiol. 2012, 158: 1666-1684. 10.1104/pp.111.192765.PubMed CentralView ArticlePubMed
- Chen YL: QTL for Traits Related with Potassium Deficiency Resistance in Rice. 2012, Chinese academy of sciences master dissertation, Beijing, China
- Liang YS: Genetic Research on Root of Populations Derived from Super Rice (Oryza sativa L.) Xieyou 9308. 2011, Chinese academy of sciences doctoral dissertation, Beijing, China
- Feng Y, Cao LY, Wu WM, Shen XH, Zhan XD, Zhai RR, Wang RC, Chen DB, Cheng SH: Mapping QTLs for nitrogen-deficiency tolerance at seedling stage in rice (Oryza sativa L.). Plant Breeding. 2010, 129: 652-656. 10.1111/j.1439-0523.2009.01728.x.View Article
- Feng Y: Genetic Analysis and QTL Mapping on the Response of A Super Rice XY9308 RIL Population to Nitrogen Levels. 2010, Shenyang agricultural university doctoral dissertation, Shenyang, China
- Wang RC: QTLMapping of Phosphorus Deficiency Tolerance in Rice (Oryza sativa L.) at Two Development Stages. 2009, Chinese academy of sciences master dissertation, Beijing, China
- Shen XH: RIL Construction and QTL Mapping for Some Traits of Super Hybrid Rice (Oryza sativa L.) XY9308. 2008, Chinese academy of sciences doctoral dissertation, Beijing, China
- Springer NM, Stupar RM: Allelic variation and heterosis in maize: How do two halves make more than a whole?. Genome Res. 2007, 17: 264-275. 10.1101/gr.5347007.View ArticlePubMed
- Li B, Dewey CN: RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics. 2011, 12: 323-10.1186/1471-2105-12-323.PubMed CentralView ArticlePubMed
- Robinson MD, McCarthy DJ, Smyth GK: edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2010, 26: 139-140. 10.1093/bioinformatics/btp616.PubMed CentralView ArticlePubMed
- Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B: Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods. 2008, 5: 621-628. 10.1038/nmeth.1226.View ArticlePubMed
- Griffing B: Use of a controlled-nutrient experiment to test heterosis hypotheses. Genetics. 1990, 126: 753-767.PubMed CentralPubMed
- Kearsey MJ, Pooni HS: The Genetical Analysis of Quantitative Traits. 1996, Chapman & Hall Press, LondonView Article
- Lynch M, Walsh B: Genetics Analysis of Quantitative Traits. 1998, Sinauer Associates Press, Sunderland
- Vuylsteke M, Van Eeuwijk F, Van Hummelen P, Kuiper M, Zabeau M: Genetic analysis of variation in gene expression in Arabidopsis thaliana. Genetics. 2005, 171: 1267-1275. 10.1534/genetics.105.041509.PubMed CentralView ArticlePubMed
- Eisen MB, Spellman PT, Brown PO, Botstein D: Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci. 1998, 95: 14863-14868. 10.1073/pnas.95.25.14863.PubMed CentralView ArticlePubMed
This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.