Abstract
Two-line hybrid rice systems represent a new technical approach to utilizing the advantages of rice hybrids. However, the mechanism underlying the male sterile-line fertility transition in rice remains unclear. Peiai 64S (PA64S) is a photoperiod- and thermo-sensitive genic male sterile (PTGMS) line in which male sterility manifests at an average temperature above 23.5 °C under long-day (LD) conditions. Nongken 58S (NK58S) is a LD-sensitive genic male sterile (PGMS) rice that is sterile under LD conditions (above 13.75 h-day). In contrast, D52S is a short-day (SD)-PGMS line that manifests male sterility under SD conditions (below 13.5 h-day). In this study, we obtained fertile and sterile plants from all three lines and performed transcriptome analyses on the anthers of the plants. Gene ontology (GO) analysis suggested that the differentially expressed genes identified were significantly enriched in common terms involved in the response to jasmonic acid (JA) and in JA biosynthesis. On the basis of the biochemical and molecular validation of dynamic, tissue-specific changes in JA, indole-3-acetic acid (IAA) levels, gibberellin (GA) levels, and JA biosynthetic enzyme activities and expression, we proposed that JA could play a pivotal role in viable pollen production through its initial upregulation, constant fluctuation and leaf-spikelet signaling under certain fertility-inducing conditions. Furthermore, we also sprayed methyl jasmonate (MEJA) and salicylhydroxamic acid (SHAM) on the plants, thereby achieving fertility reversal in the PGMS lines NK58S and D52S, with 12.91–63.53% pollen fertility changes. Through qPCR and enzyme activity analyses, we identified two key enzymes—allene oxide synthase (AOS) and allene oxide cyclase (AOC)—that were produced and upregulated by 20–500-fold in PGMS in response to spraying; the activities of these enzymes reversed pollen fertility by influencing the JA biosynthetic pathway. These results provide a new understanding of hormone interactions and networks in male-sterile rice based on the role of JA that will help us to better understand the potential regulatory mechanisms of fertility development in rice in the future.
Highlights
Rice serves as a food source for nearly 50% of the global population
We found that the jasmonic acid (JA) level and the JA biosynthetic pathway plays a pivotal role in rice pollen fertility
For both photoperiod-sensitive genic male sterile (PGMS) and photoperiod- and thermo-sensitive genic male sterile (PTGMS) rice lines, the critical stage for their male fertility transformation is from the 3rd to 7th stages, according to the eight-stage differentiation of young spikes [39]
Summary
Rice serves as a food source for nearly 50% of the global population. With the reduction in arable land and the increase in the population worldwide, hybrid rice breeding has greatly increased food production, with a 55% yield increase during recent decades [1].Among hybrid rice breeding approaches, the two-line hybrid rice breeding system was initiated and developed through the utilization of photoperiod- and thermo-sensitive genic male sterile (PTGMS) lines; this approach has many advantages, including increased yields and optimized hybrid seed production [2,3]. Rice serves as a food source for nearly 50% of the global population. With the reduction in arable land and the increase in the population worldwide, hybrid rice breeding has greatly increased food production, with a 55% yield increase during recent decades [1]. Among hybrid rice breeding approaches, the two-line hybrid rice breeding system was initiated and developed through the utilization of photoperiod- and thermo-sensitive genic male sterile (PTGMS) lines; this approach has many advantages, including increased yields and optimized hybrid seed production [2,3]. Many PTGMS rice varieties have been discovered or created, such as Nongken 58S (NK58S), Peiai 64S (PA64S), Annong S-1, Guangzhan 63S and Y58S [4,5,6,7]. A number of these varieties are widely used, with a very large production area in China, such as PA64S, Guangzhan 63S and Y58S
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