Skip to main page content
Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
, 12 (1), 34

Carbohydrate Metabolism and Fertility Related Genes High Expression Levels Promote Heterosis in Autotetraploid Rice Harboring Double Neutral Genes

Affiliations

Carbohydrate Metabolism and Fertility Related Genes High Expression Levels Promote Heterosis in Autotetraploid Rice Harboring Double Neutral Genes

Lin Chen et al. Rice (N Y).

Abstract

Background: Autotetraploid rice hybrids have great potential to increase the production, but hybrid sterility is a major hindrance in the utilization of hybrid vigor in polyploid rice, which is mainly caused by pollen abortion. Our previous study showed that double pollen fertility neutral genes, Sa-n and Sb-n, can overcome hybrid sterility in autotetraploid rice. Here, we used an autotetraploid rice line harboring double neutral genes to develop hybrids by crossing with auto- and neo-tetraploid rice, and evaluated heterosis and its underlying molecular mechanism.

Results: All autotetraploid rice hybrids, which harbored double pollen fertility neutral genes, Sa-n and Sb-n, displayed high seed setting and significant positive heterosis for yield and yield-related traits. Cytological observations revealed normal chromosome behaviors and higher frequency of bivalents in the hybrid than parents during meiosis. Transcriptome analysis revealed significantly higher expressions of important saccharides metabolism and starch synthase related genes, such as OsBEIIb and OsSSIIIa, in the grains of hybrid than parents. Furthermore, many meiosis-related and specific genes, including DPW and CYP703A3, displayed up-regulation in the hybrid compared to a parent with low seed setting. Many non-additive genes were detected in the hybrid, and GO term of carbohydrate metabolic process was significantly enriched in all the transcriptome tissues except flag leaf (three days after flowering). Moreover, many differentially expressed genes (DEGs) were identified in the yield-related quantitative trait loci (QTLs) regions as possible candidate genes.

Conclusion: Our results revealed that increase in the number of bivalents improved the seed setting of hybrid harboring double pollen fertility neutral genes. Many important genes, including meiosis-related and meiosis-specific genes and saccharides metabolism and starch synthase related genes, exhibited heterosis specific expression patterns in polyploid rice during different development stages. The functional analysis of important genes will provide valuable information for molecular mechanisms of heterosis in polyploid rice.

Keywords: Chromosome; Hybrid vigor; Neo-tetraploid rice; Polyploidy; Sterility; Transcriptome.

Conflict of interest statement

Ethics approval and consent to participate

Not applicable

Consent for publication

Not applicable

Competing interests

The authors declare that there are no conflicts of interest.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Figures

Fig. 1
Fig. 1
Comparisons of morphological characteristics between F1 hybrid and its parents. a Plant appearance of F1, T449 and H1. Pollens of T449 (b), F1 (c), and H1 (d), blue arrows indicate normal pollens, red arrows indicate abnormal pollens. Bar = 100 μm. Embryo sacs of T449 (e), F1 (f) and H1 (g), white arrows indicate antipodal cells and red arrows indicate two polar nuclei. Bar = 100 μm
Fig. 2
Fig. 2
Chromosome configuration at diakinesis and metaphase I. a-d, T449. E-H, H1. I-T, F1. a, 9IV (6 ring shape (arrow) + 1 OK shape + 2 X shape) + 2III + 2II + 2I; b, 2IV (1 ring shape + 1 chain shape (arrow)) + 2III + 14II + 6I; c, 6IV (4 ring shape + 1 chain shape (arrow) + 1 X shape) + 3III + 7II + 1I; d, 9IV (7 ring shape + 1 chain shape + 1 X shape (arrow)) + 3III + 1II + 1I; e, 9IV (6 ring shape + 1 OK shape (arrow) + 2 X shape) +6II; f, 8IV (1 ring shape + 1 chain shape+ 2 frying pan shape (arrow) + 4 X shape) +8II; g, 7IV (4 ring shape (arrow) + 1 OK shape + 2X shape) +8II + 4I; h, 9IV (5 ring shape + 4 X shape + 1 chain shape (arrow)) +6II; i, 9IV (6 ring shape + 2 frying pan shape (arrow) + 1 chain shape) + 6II; j, 6IV (4 ring shape + 1 frying pan shape (arrow) + 1 X shape) + 12II; k, 8IV (4 ring shape + 1 chain shape + 3 X shape (arrow)) + 8II; l, 8IV (5 ring shape (arrow) + 3 X shape) + 8II; m, IV (3 ring shape (arrow) + 1 frying pan shape + 1 OK shape + 1 chain shape + 2 X shape) + 8II; n, 4IV (4 ring shape (arrow)) + 15II + 2I;o, 8IV (5 ring shape + 1 frying pan shape + 1 OK shape (arrow) + 1 X shape) +8II; p, 5IV (5 ring shape (arrow)) + 14II; q, 11IV (6 ring shape + 2 frying pan shape (arrow) + 1 OK shape+ 2 X shape) + 2II; r, 8IV (3 ring shape (arrow) + 5 X shape) + 8II; s, 8IV (4 ring shape + 1 frying pan shape (arrow) + 3 X shape) + 8II; t, 6IV (4 ring shape +2 X shape (arrow)) + 11II+ 2I. Bar = 10 μm
Fig. 3
Fig. 3
Classification of chromosome configuration. a1–a4 represent ring shape, b1–b4 represent chain shape, c1–c4 represent frying pan shape, d1–d4 represent “X” shape, e1–e4 represent “OK” shape
Fig. 4
Fig. 4
Gene ontology (GO) enrichment heat map for DEGFPU in 9 tissues (GO terms were selected based on their appearance at least in three tissues or more). L1 and P1 represent flag leaves and anthers at meiosis stage, respectively. L2, P2, E2 and Z2 represent flag leaves, anther, embryo sac and leaf sheath at pre-flowering stage, respectively. L3, P3 and Z3 represent flag leaves, grain and leaf sheath at three days after flowering, respectively
Fig. 5
Fig. 5
Distribution of DEGFPU mapped onto yield-related QTLs. QTLs in Gramene (number of harbored genes ≤100) harboring DEGFPU were aligned to the Michigan State University (MSU) Rice Genome Release 6.1
Fig. 6
Fig. 6
Gene expression levels of 47 genes and predicted protein-protein interaction network. a, The distribution of 47 genes exhibited up-regulation in F1 hybrid and H1 compared to T449 and down-regulation in T449 compared to E249 during meiosis stage, b, Predicted protein-protein interaction network of differently expressed genes (black), meiosis-specific (blue) and meiosis-related (red) genes. T represents T449, F represents hybrid, and H represents H1
Fig. 7
Fig. 7
WGCNA based gene expression matrix between hybrid and parents. a Hierarchical cluster tree showing co-expression modules identified by WGCNA. Each leaf in the tree represents one gene. The major tree branches constitute 28 modules labeled with different colors. b Module-sample relationship. Each row corresponds to a module. Each column corresponds to a sample. The color of each cell at the row-column intersection indicates the correlation coefficient between the module and the sample
Fig. 8
Fig. 8
Predicted carbohydrate pathways in grains three days after flowering and related-gene variations in parents. a Starch pathway in grains of polyploid rice. The log2-transformed ratio between hybrid and parents was drawn by heatmap (F, F1 hybrid; T449, maternal line; H1, paternal line). b Sequence comparisons of OsSUS3, OsBEIIb and OsSSIIIa in T449 and H1

Similar articles

See all similar articles

Cited by 3 articles

References

    1. Adamowski EDV, Pagliarini MS, Do Valle CB. Meiotic behaviour in three interspecific three-way hybrids between Brachiaria ruziziensis and B. brizantha (Poaceae: Paniceae) J Genet. 2008;87:33–38. doi: 10.1007/s12041-008-0005-7. - DOI - PubMed
    1. Albertin W, Balliau T, Brabant P, Chevre A, Eber F, Malosse C, Thiellement H. Numerous and rapid nonstochastic modifications of gene products in newly synthesized Brassica napus allotetraploids. Genet. 2006;173:1101–1113. doi: 10.1534/genetics.106.057554. - DOI - PMC - PubMed
    1. Bai H, Cao Y, Quan J, Dong L, Li Z, Zhu Y, Zhu L, Dong Z, Li D. Identifying the genome-wide sequence variations and developing new molecular markers for genetics research by re-sequencing a landrace cultivar of foxtail millet. PLoS One. 2013;8:9. - PMC - PubMed
    1. Cai DT, Yuan LP, Lu XG. A new strategy of rice breeding in the 21st century II. Searching a new pathway of rice breeding by utilization of double heterosis of wide cross and polyploidization. Acta Agron Sin. 2001;27:110–116.
    1. Cakir B, Shiraishi S, Tuncel A, Matsusaka H, Satoh R, Singh S, Crofts N, Hosaka Y, Fujita N, Hwang SK, Satoh H, Okita TW. Analysis of the rice ADP-glucose transporter (OsBT1) indicates the presence of regulatory processes in the amyloplast stroma that control ADP-glucose flux into starch. Plant Physiol. 2016;170:1271–1283. - PMC - PubMed

LinkOut - more resources

Feedback