Heterosis associated gene expression in maize embryos 6 days after fertilization exhibits additive, dominant and overdominant pattern

Abstract

Heterosis is important for conventional plant breeding and is intensively used to increase the productivity of crop plants. Genetic processes shortly after fertilization might be of particular importance with respect to heterosis, because coordination of the diverse genomes establishes a basis for future performance of the sporophyte. Here we demonstrate a strong crossbreeding advantage of hybrid maize embryos as early as 6 days after fertilization in a modern maize hybrid and provide the first embryo specific analysis of associated gene expression pattern at this early stage of development. We identified differentially expressed genes between hybrid embryos and the parental genotypes by a combined approach of suppression subtractive hybridization and differential screening by microarray hybridizations. Association of heterosis in embryos with genes related to signal transduction and other regulatory processes was implied by the enrichment of these functional classes among the identified gene set. Quantitative RT-PCR analysis validated the expression pattern of 7 of 12 genes analysed and revealed predominantly additive, but also dominant and overdominant expression patterns in hybrid embryos. These patterns indicate that gene regulatory interactions among parental alleles act at this early developmental stage and the genes identified provide entry points for the exploration of gene regulatory networks associated with the specification of the phenomenon heterosis in the plant life cycle.

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

“…For 66% of the genes that displayed nonadditive expression in microarray experiments, this difference from additivity was confirmed in qRT-PCR experiments. This confirmation rate was similar to the values obtained for maize seedlings (Swanson-Wagner et al 2006) where among 45 genes tested in qRT-PCR 31 were confirmed to be nonadditively expressed (69%), for maize embryos where 8 of 12 (67%) nonadditively expressed genes were confirmed via qRT-PCR (Meyer et al 2007), and for shoot apical meristems where 2 of 3 genes (67%) were confirmed via qRT-PCR (Uzarowska et al 2007).…”

“…A number of studies have compared gene expression profiles of inbred lines vs. hybrids in different maize organs and developmental stages, including embryos (Stupar and Springer 2006;Meyer et al 2007), endosperm (Guo et al 2003;Song and Messing 2003), whole seedlings (Stupar and Springer 2006;Swanson-Wagner et al 2006), immature ears (Guo et al 2006;Stupar and Springer 2006), adult leaves (Auger et al 2005), and shoot apical meristem (Uzarowska et al 2007). In addition to these studies in maize, the transcriptomes of the first Arabidopsis leaf (Vuylsteke et al 2005) and rice panicles (Huang et al 2006) have been analyzed.…”

“…Heterosis was first described by Charles Darwin (Darwin 1876) and independently rediscovered by Shull (1908) and East (1908). Heterosis is most evident for adult traits like plant biomass or yield but is also apparent during embryo (Meyer et al 2007) and early seedling development .…”

“…However, in some instances the apparent loss of gene colinearity might be due to the movement of genes or gene fragments by helitron transposons to other genomic regions and thus the contribution of noncolinear regions of the genome to heterosis is unclear (Lai et al 2005). Moreover, a number of studies have compared gene expression patterns of selected genes in inbred lines and hybrids (Song and Messing 2003;Auger et al 2005;Meyer et al 2007) or examined global gene expression analyses (Guo et al 2003(Guo et al , 2006Stupar and Springer 2006;Swanson-Wagner et al 2006;Uzarowska et al 2007) to test the hypothesis that nonadditive gene expression in hybrids is associated with heterosis (Song and Messing 2003). These studies differed significantly in their experimental design, analyzed plant tissues and developmental stages, genotypes, and statistical procedures, making it difficult to compare them.…”

“…Nonadditive gene expression patterns in hybrids are significantly different from the midparent value, while additive expression patterns are not. While in some studies additive gene expression was prevalent (Stupar and Springer 2006;SwansonWagner et al 2006;Meyer et al 2007), in other studies nonadditive gene expression (Uzarowska et al 2007) or a similar number of genes that provided additive and nonadditive expression (Guo et al 2006) prevailed. Although this discrepancy in global gene expression patterns might be related to the different experimental approaches this could also be an indication of different global expression patterns in different tissues and developmental stages that might nevertheless be related to heterosis (Hochholdinger and Hoecker 2007).…”