Early changes of gene activity in developing seedlings of Arabidopsis hybrids relative to parents may contribute to hybrid vigour

Hybrid vigour (heterosis) has been used for decades in crop industries, especially in the production of maize and rice. Hybrid varieties usually exceed their parents in plant biomass and seed yield. But the molecular basis of hybrid vigour is not fully understood. In this project, we studied heterosis at early stages of seedling development in Arabidopsis hybrids derived from crossing Ler and C24 accessions. We found that early heterosis is associated with non‐additive gene expression that resulted from earlier changes in gene expression in the hybrids relative to the parents. The non‐additively expressed genes are involved in metabolic pathways, including photosynthesis, critical for plant growth. The early increased expression levels of genes involved in energy production in hybrids is associated with heterosis in the young seedlings that could be essential for biomass heterosis at later developmental stages of the plant.     

Genome‐wide identification and analysis of heterotic loci in three maize hybrids

Heterosis, or hybrid vigour, is a predominant phenomenon in plant genetics, serving as the basis of crop hybrid breeding, but the causative loci and genes underlying heterosis remain unclear in many crops. Here, we present a large‐scale genetic analysis using 5360 offsprings from three elite maize hybrids, which identifies 628 loci underlying 19 yield‐related traits with relatively high mapping resolutions. Heterotic pattern investigations of the 628 loci show that numerous loci, mostly with complete–incomplete dominance (the major one) or overdominance effects (the secondary one) for heterozygous genotypes and nearly equal proportion of advantageous alleles from both parental lines, are the major causes of strong heterosis in these hybrids. Follow‐up studies for 17 heterotic loci in an independent experiment using 2225 F₂ individuals suggest most heterotic effects are roughly stable between environments with a small variation. Candidate gene analysis for one major heterotic locus (ub3) in maize implies that there may exist some common genes contributing to crop heterosis. These results provide a community resource for genetics studies in maize and new implications for heterosis in plants.     

玉米雌穗发育期基因差异表达与杂种优势的研究

杂种优势在提高粮食作物特别是玉米的产量方面具有重要的作用。然而,杂种优势的原理却仍然是一个世界性的难题。用12个玉米自交系及其按不完全双列杂交组配的33个杂交种为材料,分4个不同发育时期取杂交种及其亲本的雌穗组织,利用差异显示技术,分析杂种与亲本的基因差异表达类型及其与7个主要农艺性状的杂种表现和杂种优势的相关关系。发现1):在5种表达类型中单态表达(基因在杂交种和双亲中同时表达的类型)的数量最大,这说明杂种优势的形成不仅与基因的表达与否相关,还与大量基因的上调或下调表达相关;2):在玉米雌幼穗的发育初期杂交种与双亲的基因表达差异最大,这可能与雌穗发育初期器官的形成和发育相关,因此这一时期差异表达(在质的方面)的基因对产量性状和杂种优势的形成具有密切关系;3):综合各种基因表达类型与产量性状和杂种优势的关系,发现某些基因在杂种中的沉默表达可以促进籽粒的发育和抑制幼穗中小花的发育。     

Allele-specific expression patterns reveal biases and embryo-specific parent-of-origin effects in hybrid maize

We employed allele-specific expression (ASE) analyses to document biased allelic expression in maize (Zea mays). A set of 316 quantitative ASE assays were used to profile the relative allelic expression in seedling tissue derived from five maize hybrids. The different hybrids included in this study exhibit a range of heterosis levels; however, we did not observe differences in the frequencies of allelic bias. Allelic biases in gene expression were consistently observed for approximately 50% of the genes assayed in hybrid seedlings. The relative proportion of genes that exhibit cis- or trans-acting regulatory variation was very similar among the different genotypes. The cis-acting regulatory variation was more prevalent and resulted in greater expression differences than trans-acting regulatory variation for these genes. The ASE assays were further used to compare the relative expression of the B73 and Mo17 alleles in three tissue types (seedling, immature ear, and embryo) derived from reciprocal hybrids. These comparisons provided evidence for tissue-specific cis-acting variation and for a slight maternal expression bias in approximately 20% of genes in embryo tissue. Collectively, these data provide evidence for prevalent cis-acting regulatory variation that contributes to biased allelic expression between genotypes and between tissues.     

Absence of heterosis in hybrid corn. Description of the effect

Three unrelated homozygous maize lines, TS11, P22, and ST156, that produced hybrids in which heterosis was either absent or insignificant were identified. These hybrids were phenotypically similar to self-pollinated homozygous lines. Reciprocal crosses showed that the absence of heterosis is controlled by nuclear genes and is not associated with the cytoplasm of inbred lines. Analysis of F2 plants demonstrated that lines TS11, P22, and ST156 contained allelic genes determining the absence of heterosis in hybrid plants. Crosses of lines TS11, P22, and ST156 with a common selection line 092 generated hybrids with normal heterosis. It was concluded that heterozygosity or homozygosity of particular genes in lines TS11, P22, and ST156 play a pivotal role in the manifestation or the absence of hybrid vigor in hybrids.     

Predictive potential of DNA markers in heterosis breeding of maize

PCR-analysis of maize inbred lines has been carried out. Genetic distances between the lines have been calculated, allelic composition and heterosis level of F-hybrids have been determined. Heterosis level of hybrid seed yield rised according to increasing of genetic distances between initial lines. Correlation of allelic composition of inbred line microsatellite loci and heterosis level of the respective hybrids has been revealed.     

Assembly of yield heterosis of an elite rice hybrid is promising by manipulating dominant quantitative trait loci

In the past, rice hybrids with strong heterosis have been obtained empirically, by developing and testing thousands of combinations. Here, we aimed to determine whether heterosis of an elite hybrid could be achieved by manipulating major quantitative trait loci. We used 202 chromosome segment substitution lines from the elite hybrid Shanyou 63 to evaluate single segment heterosis (SSH) of yield per plant and identify heterotic loci. All nine detected heterotic loci acted in a dominant fashion, and no SSH exhibited overdominance. Functional alleles of key yield-related genes Ghd7, Ghd7.1, Hd1, and GS3 were dispersed in both parents. No functional alleles of three investigated genes were expressed at higher levels in the hybrids than in the more desirable parents. A hybrid pyramiding eight heterotic loci in the female parent Zhenshan 97 background had a comparable yield to Shanyou 63 and much higher yield than Zhenshan 97. Five hybrids pyramiding eight or nine heterotic loci in the combined parental genome background showed similar yield performance to that of Shanyou 63. These results suggest that dominance underlying functional complementation is an important contributor to yield heterosis and that heterosis assembly might be successfully promised by manipulating several major dominant heterotic loci.     

Specific changes in total and mitochondrial proteomes are associated with higher levels of heterosis in maize hybrids

The phenomenon of hybrid vigor (heterosis) has long been harnessed by plant breeders to improve world food production. However, the changes that are essential for heterotic responses and the mechanisms responsible for heterosis remain undefined. Large increases in biomass and yield in high-heterosis hybrids suggest that alterations in bioenergetic processes may contribute to heterosis. Progeny from crosses between various inbred lines vary in the extent of vigor observed. Field-grown maize F(1) hybrids that consistently exhibited either low or high heterosis across a variety of environments were examined for changes in proteins that may be correlated with increased plant vigor and yield. Unpollinated ears at the time of flowering (ear shoots) were selected for the studies because they are metabolically active, rich in mitochondria, and the sizes of the ears are diagnostic of yield heterosis. Total protein and mitochondrial proteomes were compared among low- and higher-heterosis hybrids. Two-dimensional difference gel electrophoresis was used to identify allelic and/or isoform differences linked to heterosis. Identification of differentially regulated spots by mass spectrometry revealed proteins involved in stress responses as well as primary carbon and protein metabolism. Many of these proteins were identified in multiple spots, but analysis of their abundances by label-free mass spectrometry suggested that most of the expression differences were due to isoform variation rather than overall protein amount. Thus, our proteomics studies suggest that expression of specific alleles and/or post-translational modification of specific proteins correlate with higher levels of heterosis.     

Comparison of maize (Zea mays L.) F1-hybrid and parental inbred line primary root transcriptomes suggests organ-specific patterns of nonadditive gene expression and conserved expression trends

The phenomenon of heterosis describes the increased agronomic performance of heterozygous F(1) plants compared to their homozygous parental inbred plants. Heterosis is manifested during the early stages of root development in maize. The goal of this study was to identify nonadditive gene expression in primary roots of maize hybrids compared to the average expression levels of their parental inbred lines. To achieve this goal a two-step strategy was used. First, a microarray preselection of nonadditively expressed candidate genes was performed. Subsequently, gene expression levels in a subset of genes were determined via high-throughput quantitative real-time (qRT)-PCR experiments. Initial microarray experiments identified 1941 distinct microarray features that displayed nonadditive gene expression in at least 1 of the 12 analyzed hybrids compared to the midparent value of their parental inbred lines. Most nonadditively expressed genes were expressed between the parental values (>89%). Comparison of these 1941 genes with nonadditively expressed genes identified in maize shoot apical meristems via the same experimental procedure in the same genotypes revealed significantly less overlap than expected by pure chance. This finding suggests organ-specific patterns of nonadditively expressed genes. qRT-PCR analyses of 64 of the 1941 genes in four different hybrids revealed conserved patterns of nonadditively expressed genes in different hybrids. Subsequently, 22 of the 64 genes that displayed nonadditive expression in all four hybrids were analyzed in 12 hybrids that were generated from four inbred lines. Among those genes a superoxide dismutase 2 was expressed significantly above the midparent value in all 12 hybrids and might thus play a protective role in heterosis-related antioxidative defense in the primary root of maize hybrids. The findings of this study are consistent with the hypothesis that both global expression trends and the consistent differential expression of specific genes contribute to the organ-specific manifestation of heterosis.     

The regulatory network mediated by circadian clock genes is related to heterosis in rice

Exploitation of heterosis in rice(Oryza sativa L.) has contributed greatly to global food security.In this study,we generated three sets of reciprocal F1 hybrids of indica and japonica subspecies to evaluate the relationship between yield heterosis and the circadian clock.There were no differences in trait performance or heterosis between the reciprocal hybrids,indicating no maternal effects on heterosis.The indica-indica and indica-japonica reciprocal F1 hybrids exhibited pronounced heterosis for chlorophyll and starch content in leaves and for grain yield/biomass.In contrast,the japonica-japonica F1 hybrids showed low heterosis.The three circadian clock genes investigated expressed in an above-high-parent pattern(AHP)at seedling stage in all the hybrids.The five genes downstream of the circadian clock,and involved in chlorophyll and starch metabolic pathways,were expressed in AHP in hybrids with strong better-parent heterosis(BPH).Similarly,three of these Research Arfive genes in the japonica-japonica F1 hybrids showing low BPH were expressed in positive overdominance,but the other two genes were expressed in additive or negative overdominance.These results indicated that the expression patterns of circadian clock genes and their downstream genes are associated with heterosis,which suggests that the circadian rhythm pathway may be related to heterosis in rice.     

Cis-transcriptional variation in maize inbred lines B73 and Mo17 leads to additive expression patterns in the F1 hybrid

Microarray analysis of gene expression patterns in immature ear, seedling, and embryo tissues from the maize inbred lines B73 and Mo17 identified numerous genes with variable expression. Some genes had detectable expression in only one of the two inbreds; most of these genes were detected in the genomic DNA of both inbreds, indicating that the expression differences are likely caused by differential regulation rather than by differences in gene content. Gene expression was also monitored in the reciprocal F1 hybrids B73xMo17 and Mo17xB73. The reciprocal F1 hybrid lines did not display parental effects on gene expression levels. Approximately 80% of the differentially expressed genes displayed additive expression patterns in the hybrids relative to the inbred parents. The approximately 20% of genes that display nonadditive expression patterns tend to be expressed at levels within the parental range, with minimal evidence for novel expression levels greater than the high parent or less than the low parent. Analysis of allele-specific expression patterns in the hybrid suggested that intraspecific variation in gene expression levels is largely attributable to cis-regulatory variation in maize. Collectively, our data suggest that allelic cis-regulatory variation between B73 and Mo17 dictates maintenance of inbred allelic expression levels in the F1 hybrid, resulting in additive expression patterns.     

A unifying theory for general multigenic heterosis: energy efficiency, protein metabolism, and implications for molecular breeding

Hybrids between genetically diverse varieties display enhanced growth, and increased total biomass, stress resistance and grain yield. Gene expression and metabolic studies in maize, rice and other species suggest that protein metabolism plays a role in the growth differences between hybrids and inbreds. Single trait heterosis can be explained by the existing theories of dominance, overdominance and epistasis. General multigenic heterosis is observed in a wide variety of different species and is likely to share a common underlying biological mechanism. This review presents a model to explain differences in growth and yield caused by general multigenic heterosis. The model describes multigenic heterosis in terms of energy-use efficiency and faster cell cycle progression where hybrids have more efficient growth than inbreds because of differences in protein metabolism. The proposed model is consistent with the observed variation of gene expression in different pairs of inbred lines and hybrid offspring as well as growth differences in polyploids and aneuploids. It also suggests an approach to enhance yield gains in both hybrid and inbred crops via the creation of an appropriate computational analysis pipeline coupled to an efficient molecular breeding program.