PIF and miR408-regulated phytocyanin module PCY-SAG14 promotes dark-induced leaf senescence in Arabidopsis

Importance

Leaf senescence is a critical process in plants and has a direct impact on many important agronomic traits. Despite decades of research, the identity of the senescence signal and the molecular mechanism that perceives and transduces the signal remain elusive. Using dark-induced leaf senescence as an experimental system, we found that senescence induces rapid reciprocal regulation of plastocyanin, a copper-binding electron transporter in the photosynthetic electron transport chain, and the PCY-SAG14 pair of phytocyanins located on the endomembrane. We also found that PCY-SAG14, which is modulated by PIF3/4/5 and miR408, is both necessary and sufficient to promote senescence. These results indicate that intracellular copper homeostasis mediated by the PCY-SAG14 module plays an important regulatory role in dark-induced leaf senescence.

Summary

Leaf senescence is a critical process in plants and has a direct impact on many important agronomic traits. Despite decades of research on senescence-modified mutants via forward genetics and functional assessment of senescence-associated genes (SAGs) via reverse genetics, the signal of senescence and the molecular mechanism that perceives and transduces the signal remain elusive. Here, using dark-induced senescence (DIS) of Arabidopsis leaf as an experimental system, we show that exogenous copper induces senescence syndrome and transcriptomic changes in light-grown plants paralleling those of DIS. By profiling transcriptomes and tracking the subcellular distribution of copper, we found that the reciprocal regulation of plastocyanin, the mobile electron transporter of thylakoid lumen in the Z-pattern of photosynthetic electron transport, and SAG14 and plantacyanin (PCY), a pair of small interacting blue copper proteins located on the endomembrane, is a common thread in different scenarios of leaf senescence, including DIS. Genetic and molecular experiments have confirmed that the PCY-SAG14 module is necessary and sufficient to promote DIS. We also found that the PCY-SAG14 module is repressed by a conserved microRNA, miR408, which in turn is repressed by the phytochrome interaction factor 3/4/5 (PIF3/4/5), the key trio of factors of transcription favoring DIS. Together, these results indicate that PCY-SAG14-mediated intracellular copper redistribution has a regulatory role in DIS. A more in-depth deciphering of the mechanism of copper homeostasis and its interaction with other pathways regulating senescence should lead to a better understanding of the fundamental question of plant aging.

Footnotes

    • Accepted December 8, 2021.
  • Author contributions: research designed by XWD and LL; CH, YY and JD conducted research; CH analyzed the data; and CH and LL wrote the article.

  • Assessors: GC, Korea Advanced Institute of Science and Technology; S.-SG, Cornell University; HG, Southern University of Science and Technology.

  • The authors declare no competing interests.

  • This article contains additional information online at https://www.pnas.org/lookup/suppl/doi:10.1073/pnas.2116623119/-/DCSupplemental.

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