Translational regulation plasticity shapes wheat grain adaptation to heat stress

Extremely high temperatures due to global warming are increasingly threatening crop production, and plants have evolved highly sophisticated mechanisms to respond to harsh environmental stresses and survive. At the translational level, how bread wheat responds to high temperatures remains largely unknown.

We use ribosome profiling and high-throughput sequencing to investigate the translatome of wheat grains in response to high temperatures. Our study reveals that heat stress profoundly reshapes the translatomic landscapes, significantly affecting the translation of the mRNAs involved in the translation process, grain development, and heat stress response. A subset of the upstream open reading frames (uORFs) and RNA-binding proteins specifically link to their potential target with associated translatomic changes under high temperature. Divergent translation of duplicated genes is affected by the imbalanced expression of uORFs. Interestingly, the high temperature stimulates expression of small ORFs in long non-coding RNAs (lORFs). Microproteins encoded by key heat-responsive lORFs localize to cellular regions including the nucleus, endoplasmic reticulum, and P-body, and interact with heat shock proteins. Furthermore, the microprotein and RNA-binding protein contribute to the heat tolerance variation among wheat accessions.

This study provides new insights into the translational regulatory mechanism in wheat heat tolerance, accelerating genetic improvements in crops for optimal climate resilience.