Polyploidy Enhances F1 Pollen Sterility Loci Interactions That Increase Meiosis Abnormalities and Pollen Sterility in Autotetraploid Rice.
Intersubspecific autotetraploid rice (Oryza sativa ssp. indica × japonica) hybrids have greater biological and yield potentials than diploid rice. However, the low fertility of intersubspecific autotetraploid hybrids, which is largely caused by high pollen abortion rates, limits their commercial utility. To decipher the cytological and molecular mechanisms underlying allelic interactions in autotetraploid rice, we developed an autotetraploid rice hybrid that was heterozygous (S(i)S(j)) at F1 pollen sterility loci (Sa, Sb, and Sc) using near-isogenic lines. Cytological studies showed that the autotetraploid had higher percentages (>30%) of abnormal chromosome behavior and aberrant meiocytes (>50%) during meiosis than did the diploid rice hybrid control. Analysis of gene expression profiles revealed 1,888 genes that were differentially expressed between the autotetraploid and diploid hybrid lines at the meiotic stage, among which 889 and 999 were up- and down-regulated, respectively. Of the 999 down-regulated genes, 940 were associated with the combined effect of polyploidy and pollen sterility loci interactions (IPE). Gene Ontology enrichment analysis identified a prominent functional gene class consisting of seven genes related to photosystem I (Gene Ontology 0009522). Moreover, 55 meiosis-related or meiosis stage-specific genes were associated with IPE in autotetraploid rice, including Os02g0497500, which encodes a DNA repair-recombination protein, and Os02g0490000, which encodes a component of the ubiquitin-proteasome pathway. These results suggest that polyploidy enhances epistatic interactions between alleles of pollen sterility loci, thereby altering the expression profiles of important meiosis-related or meiosis stage-specific genes and resulting in high pollen sterility.
State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, South China Agricultural University, Guangzhou 510642, China.
Jinwen
J
Wu
State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, South China Agricultural University, Guangzhou 510642, China.
Muhammad Qasim
http://orcid.org/0000-0002-6767-4355
MQ
Shahid
State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, South China Agricultural University, Guangzhou 510642, China.
Lin
L
Chen
State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, South China Agricultural University, Guangzhou 510642, China.
Zhixiong
Z
Chen
State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, South China Agricultural University, Guangzhou 510642, China.
Lan
L
Wang
State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, South China Agricultural University, Guangzhou 510642, China xdliu@scau.edu.cn yglu@scau.edu.cn.
Xiangdong
http://orcid.org/0000-0003-1568-1745
X
Liu
State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, South China Agricultural University, Guangzhou 510642, China xdliu@scau.edu.cn yglu@scau.edu.cn.
Yonggen
Y
Lu
D000483:Alleles; D018533:Biomass; D032461:Chromosomes, Plant / Q000235:genetics; D016000:Cluster Analysis; D004171:Diploidy; D004843:Epistasis, Genetic; D020869:Gene Expression Profiling; D018506:Gene Expression Regulation, Plant; D063990:Gene Ontology; D053263:Gene Regulatory Networks / Q000235:genetics; D017343:Genes, Plant / Q000235:genetics; D006824:Hybridization, Genetic; D008540:Meiosis / Q000235:genetics*; D020411:Oligonucleotide Array Sequence Analysis / Q000379:methods; D012275:Oryza / Q000235:genetics* / Q000378:metabolism; D051479:Plant Infertility / Q000235:genetics*; D011058:Pollen / Q000235:genetics*; D011123:Polyploidy; D060066:Protein Interaction Maps / Q000235:genetics; D020133:Reverse Transcriptase Polymerase Chain Reaction