Priming of retrograde signaling in wheat across multiple natural environments reveal how responses to dynamic stimuli can be integrated to alter yield, yield stability and water productivity

Chloroplasts act as environmental sensors, enabling rapid plant stress responses through operational retrograde signaling. While these signals operate on minutes-to-hours’ time scales, their cumulative impact and function across a plant’s lifecycle and in field conditions remains unknown.

We investigated if retrograde signaling’s transient changes to gene expression have cumulative effects by generating wheat mutants with primed SAL1-PAP retrograde pathway responsiveness. After confirming changes in photosynthesis and drought resilience under controlled conditions, we conducted 15 field trials across South-Eastern Australia, spanning diverse environments with varying temperatures, rainfall, and light conditions, analysing physiological responses, yield, biomass, and water productivity.

We found gene locus-specific effects on biomass, yield, and water productivity. Multi-environment analysis showed the SAL-4A locus was more strongly associated with improved performance, with the converse for SAL-5D. Significantly, modulation of specific SAL subtypes enhanced photosynthetic efficiency and stress resilience while improving average yields by 4 and 8% respectively for 4A loci across 15 field sites, challenging the traditional yield-resilience trade-off paradigm.

This study reveals retrograde signals operate in field environments, integrating environmental information across a plant’s lifecycle to improve yield, water productivity and dynamic acclimation to diverse growing seasons, and highlight the importance of multi-environment field validation for crop modifications.