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Complementation contributes to transcriptome complexity in maize (Zea mays L.) hybrids relative to their inbred parents.

ABSTRACT: Typically, F(1)-hybrids are more vigorous than their homozygous, genetically distinct parents, a phenomenon known as heterosis. In the present study, the transcriptomes of the reciprocal maize (Zea mays L.) hybrids B73×Mo17 and Mo17×B73 and their parental inbred lines B73 and Mo17 were surveyed in primary roots, early in the developmental manifestation of heterotic root traits. The application of statistical methods and a suitable experimental design established that 34,233 (i.e., 86%) of all high-confidence maize genes were expressed in at least one genotype. Nearly 70% of all expressed genes were differentially expressed between the two parents and 42%-55% of expressed genes were differentially expressed between one of the parents and one of the hybrids. In both hybrids, ?10% of expressed genes exhibited nonadditive gene expression. Consistent with the dominance model (i.e., complementation) for heterosis, 1124 genes that were expressed in the hybrids were expressed in only one of the two parents. For 65 genes, it could be shown that this was a consequence of complementation of genomic presence/absence variation. For dozens of other genes, alleles from the inactive inbred were activated in the hybrid, presumably via interactions with regulatory factors from the active inbred. As a consequence of these types of complementation, both hybrids expressed more genes than did either parental inbred. Finally, in hybrids, ?14% of expressed genes exhibited allele-specific expression (ASE) levels that differed significantly from the parental-inbred expression ratios, providing further evidence for interactions of regulatory factors from one parental genome with target genes from the other parental genome.

SUBMITTER: Paschold A

PROVIDER: S-EPMC3514674 | biostudies-literature | 2012 Dec

REPOSITORIES: biostudies-literature

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Complementation contributes to transcriptome complexity in maize (Zea mays L.) hybrids relative to their inbred parents.

Paschold Anja A Jia Yi Y Marcon Caroline C Lund Steve S Larson Nick B NB Yeh Cheng-Ting CT Ossowski Stephan S Lanz Christa C Nettleton Dan D Schnable Patrick S PS Hochholdinger Frank F

Genome research 20121019 12

Typically, F(1)-hybrids are more vigorous than their homozygous, genetically distinct parents, a phenomenon known as heterosis. In the present study, the transcriptomes of the reciprocal maize (Zea mays L.) hybrids B73×Mo17 and Mo17×B73 and their parental inbred lines B73 and Mo17 were surveyed in primary roots, early in the developmental manifestation of heterotic root traits. The application of statistical methods and a suitable experimental design established that 34,233 (i.e., 86%) of all hi ...[more]

PMID: 23086286

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Project description:In this study expression levels of 732 genes were analyzed for European maize (Zea mays L.) inbred lines (4 Flint and 5 Dent) and nine corresponding hybrids by microarray analysis. The selection of the 732 genes was based on a previous study (Thiemann et al., Theor Appl Genet 2010, 120:401-413), which sequences were derived from the 46k microarray (platform GPL6438) (University of Arizona, USA). 558 of the 732 genes represented on the microarray were differentially expressed between the original 21 parental inbred lines and were correlated with at least one of the three characteristics MPH (mid-parent heterosis) and/or HP (hybrid performance) of the trait GY (grain yield) and/or HP of the trait grain dry matter content. Some of those correlated genes show overlapping correlations. The residual 174 non-correlated genes belong to the top 6 biological processes that were found to be enriched among the HP for GY-correlated genes (Thiemann et al., Theor Appl Genet 2010, 120:401M-bM-^@M-^S413). The aim of this study was the identification of the hybrid expression pattern of the subset of genes, which mid-parental expression levels were shown to be correlated with MPH for GY or showed no correlation. For the analysis total RNA of 7-day old seedlings was extracted and amino-allyl-labeled RNA was synthesized. The microarrays were scanned (AppliedPrecision ArrayWorx Scanner, Applied Precision Inc., USA) and data were evaluated using the Software GenePix Pro 4.0 (Molecular Devices, Sunnyvale, USA). Hybridizations were conducted between each pair of parental inbred lines and its corresponding hybrids. In total 4 biological replicates per genotype were analyzed. As a result 119 (22.9 %) of the 519 MPH for GY or non-correlated genes showed differential expression in at least one of the nine inbred-hybrid comparisons. These differentially expressed genes were further analyzed for hybrid expression, resulting in a mainly additive expression. Of all differential expression, additive expression of 86.21 % (with 13.79 % non-additive) of the MPH-correlated genes, and a slightly smaller contingent of 79.66 % (with 20.34 % non-additive) of the non-correlated genes was measured. Four biological replicates of each of the nine parental inbred lines (4 Flint: F012, F039, F047, L024; 5 Dent: S028, S036, P024, P033, P048) and of the nine corresponding hybrids (P033xF047, P048xF047, P024xF039, S036xL024, S028xL024, S028xF012, S028xF039, P024xF012, F012xF039) were grown under controlled conditions (25 M-BM-0C 16 h day, 21 M-BM-0C 8 h night, 70 % air humidity) for seven days in a climate chamber. Whole seedlings were frozen in liquid nitrogen and were finely pounded. Total RNA was extracted and then precipitated (4 M LiCl). Residual genomic DNA was hydrolyzed with DNaseI (Fermentas, St. Leon-Rot, Germany) and purified with the M-bM-^@M-^\NucleoSpin RNA Clean-up KitM-bM-^@M-^] (Macherey-Nagel, DM-CM-<ren, Germany). For first strand cDNA synthesis, 5 M-BM-5g of total RNA and the Superscript II from Invitrogen (Life Technologies, Carlsbad, USA) were used. Second strand synthesis was performed using DNA Polymerase I and RNase H followed by a 5 min incubation step of T4 DNA Polymerase (Fermentas, St. Leon-Rot). Residual RNA was hydrolyzed with RNase A. In-vitro transcription was performed with the T7 RNA Polymerase (Fermentas, St. Leon-Rot, Germany) for 4 h to incorporate aminoallyl-labeled UTPs (Fermentas, St. Leon-Rot, Germany). Finally, residual DNA was degraded with DNase I (Fermentas). Synthesized aaRNA was coupled with fluorescence dyes Cy3 or Cy5 (GE Healthcare, Chalfont St. Giles, UK). The RNeasy MinElute Kit (Qiagen, Hilden, Germany) was used for purification and removal of unbound dye. In total 105 hybridizations were realized. The dye used for each biological replicate of each genotype was alternated to reduce systematic bias.

Project description:Waterlogging is an important abiotic stress constraint that causes significant yield losses in maize grown throughout south and south-east Asia due to erratic rainfall patterns. The most economic option to offset the damage caused by waterlogging is to genetically incorporate tolerance in cultivars that are grown widely in the target agro-ecologies. We assessed the genetic variation in a population of recombinant inbred lines (RILs) derived from crossing a waterlogging tolerant line (CAWL-46-3-1) to an elite but sensitive line (CML311-2-1-3) and observed significant range of variation for grain yield (GY) under waterlogging stress along with a number of other secondary traits such as brace roots (BR), chlorophyll content (SPAD), % stem and root lodging (S&RL) among the RILs. Significant positive correlation of GY with BR and SPAD and negative correlation with S&RL indicated the potential use of these secondary traits in selection indices under waterlogged conditions. RILs were genotyped with 331 polymorphic single nucleotide polymorphism (SNP) markers using KASP (Kompetitive Allele Specific PCR) Platform. QTL mapping revealed five QTL on chromosomes 1, 3, 5, 7 and 10, which together explained approximately 30% of phenotypic variance for GY based on evaluation of RIL families under waterlogged conditions, with effects ranging from 520 to 640 kg/ha for individual genomic regions. 13 QTL were identified for various secondary traits associated with waterlogging tolerance, each individually explaining from 3 to 14% of phenotypic variance. Of the 22 candidate genes with known functional domains identified within the physical intervals delimited by the flanking markers of the QTL influencing GY and other secondary traits, six have previously been demonstrated to be associated with anaerobic responses in either maize or other model species. A pair of flanking SNP markers has been identified for each of the QTL and high throughput marker assays were developed to facilitate rapid introgression of waterlogging tolerance in tropical maize breeding programs.

Dataset Information

Complementation contributes to transcriptome complexity in maize (Zea mays L.) hybrids relative to their inbred parents.

Publications

Complementation contributes to transcriptome complexity in maize (Zea mays L.) hybrids relative to their inbred parents.

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