Reduced plant height can greatly improve lodging resistance, harvest index and yield potential in wheat. The “Green Revolution (GR)” genes, Rht-B1b and Rht-D1b, have been widely used in wheat breeding. However, the GR genes reduce grain weight, coleoptile length and seed vigor, which has adverse effects on seedling emergence, and significantly increase susceptibility to Fusarium head blight (FHB). Therefore, it is important to identify alternative reduced plant height genes.

Here we mapped a major QTL RHT24 for plant height in a recombinant inbred line population derived from a cross of elite wheat varieties Jingdong 8 (JD8) and Aikang 58 (AK58). Genetic analyses showed that the semi-dwarfing allele Rht24b in AK58 significantly reduced plant height without adverse effects on FHB resistance and coleoptile length compared with the tall allele Rht24a in JD8. Positional cloning identified TaGA2ox-A9 as the causal gene of RHT24. Rht24b conferred significantly higher expression of TaGA2ox-A9 and reduced plant height by lowering bioactive gibberellin levels and cell size in stem internodes. Phenotypic investigations of transgenic and near-isogenic lines demonstrated that Rht24b reduced plant height without yield penalty, which is confirmed by association analysis in a natural population. To explore the underlying mechanisms of Rht24b in reducing plant height without yield penalty, we performed molecular and physiological analyses and found that Rht24b promoted nitrogen utilization efficiency and photosynthetic capacity as well as the expression of related genes. Rht24b also up-regulated GA20 oxidase genes and down-regulated GA20 oxidase genes in leaves, suggesting that it could trigger a negative feedback regulation of GA homeostasis. Strikingly, Rht24b caused a reduced bioactive GA in stems but an elevated bioactive GA isoforms in leaves at the jointing stage. Thus TaGA2ox-A9 not only regulates bioactive GA metabolism but also modulates spatio-temporal distribution of bioactive GA. Some studies reported that GA can increase nitrogen content and photosynthesis in plants, so it appeared that Rht24b-caused enhancement of bioactive GA in leaves promoted nitrogen utilization efficiency and photosynthetic capacity. These results can explain the function of Rht24b in reducing plant height without negative effect on yield. Additionally, we investigated genetic variation at the RHT24 locus in a wide range of germplasm and traced the origin, spread and distribution of Rht24b. Sequencing and genotyping assays revealed that Rht24b first appeared in wild emmer, a progenitor of common wheat, and also occurred at a much higher frequency (74.3%) than Rht-B1b (29.5%) or Rht-D1b (33.0%) in 1,000 wheat varieties from various countries. Rht24b was detected in more than half of the investigated wild emmer and wheat accessions, suggesting that it predated the GR genes and was subjected to positive selection naturally and artificially. Many widely grown wheat varieties contained Rht24b instead of Rht-B1b and Rht-D1b. Thus Rht24b is an ancestral GR gene and still has great potential in the modern wheat breeding. Overall, these findings not only uncover an important genetic resource but also provide useful clues for dissection of the regulatory mechanisms underlying gibberellin-mediated morphogenesis and yield formation.