In a study published in Cell on May 22, research group of Prof. Chuanyou Li, from Shandong Agricultural University reported their discovery that REGENERATION FACTOR1 (REF1) is a local wound signal promoting plant regeneration, and the application of REF1 enhances the transformation efficiency of recalcitrant crops by boosting their regeneration capacity
Living organisms are often exposed to a wide range of biotic and abiotic stresses that cause severe wounding, leading to partial or complete organ loss. Upon injury, both plants and animals are able to regenerate new tissues or organs to minimize the impact of regular wear and tear.Compare to their animal counterparts, plants encounter injuries more frequently and have evolved a remarkable regenerative capacity to repair damaged tissues and to regenerate new organs or whole plants. Upon injury, plants immediately activate defense responses to prevent pathogen infection and/or insect attack. In parallel, plants activate cellular reprogramming to repair damaged tissues and regenerate lost body parts.
Notably, the signaling mechanisms orchestrating wound-induced defense responses has been intensively studied in the tomato model. Here, the peptide signal systemin and the plant hormone jasmonate regulate plant systemic defense responses through a common signaling pathway.
Whereas the wound signals and their signaling cascades used by plants to activate wound-induced defense responses have been well studied, the molecular mechanisms underlying wound-triggered regenerative responses remain obscure. Despite wounding is essential to initiate various types of organ regeneration, the biochemical nature of the putative local wound signals governing this process remains enigmatic for centuries. Furthermore, the plant regenerative capacity in nature varies widely among species and genotypes, which represents one of the biggest hurdles to fully realizing the application potential of genetic transformation and genome editing technologies for crop breeding. Therefore, among 125 important unknown questions published by Science, “what controls organ regeneration” was selected as one of the most important 25 questions.
Considering that regeneration and defense are interconnected facets of the plant wound responses, it is reasonable to speculate that tomato mutants that are defective in the putative regeneration signal would display both compromised regeneration capacity as well as impaired defense responses. Based on this principle, the researchers identified the spr9 mutant that is defective in both wound-induced defense responses and regenerative responses. spr9 primarily affects local defense responses and abolishes the capacity of wound-induced callus formation and shoot regeneration,suggesting that the SPR9 gene plays a dual role in regulating wounding-triggered local defense and organ regeneration.
Gene cloning studies revealed that the SPR9 gene encodes a precursor of a peptide. Depletion of SPR9 abolished the regeneration capacity of tomato, overexpression of SPR9 led to enhanced regeneration capacity. Moreover, application of its peptide product dramatically increased regeneration capacity. Therefore, this peptide was designated as REGENERATION FACTOR1, REF1.
Further studies demonstrated that REF1 is perceived by the receptor PORK1. When plant cells are injured, REF1 binds its receptor PORK1 to activate WIND1, a master regulator of wound-induced cellular reprogramming, thereby initiating regenerative responses. Meanwhile, activated WIND1 binds the promoter of the REF1 precursor gene to activate its expression, thereby amplifying the REF1 signaling for tissue repair and organ regeneration. Thus, REF1 acts as a phytocytokine to orchestrate wound-triggered organ regeneration.
Peptide REF1 is a local wound signal promoting plant regeneration
Since REF1 and its receptor are broadly conserved in both dicot and monocot plants, REF1-induced enhancement of regeneration capacity is a widespread mechanism. Application of REF1 dramatically enhanced the transformation efficiency of multiple difficult-to-transform crops, including soybean, wheat, and maize.
REF1 boosts regeneration and transformation efficiency of recalcitrant crops
Discovery of REF1 not only answers the long-standing question of how plants initiate organ regeneration, but also provides a convenient and universal method to boost the transformation efficiency of crops in a species- and/or genotype-independent manner.
This study was funded by the National Natural Science Foundation of China, the National Key Research and Development Program of China, and the Taishan Academy of Tomato Innovation.
Contact:
Prof. Chuanyou Li
College of Life Sciences, Shandong Agricultural University
Email: cyli@genetics.ac.cn
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1.Yang W#, Zhai H#, Wu F#, Deng L#,*, Chao Y, Meng X, Chen Q, Liu C, Bie X, Sun C, Yu Y, Zhang X, Zhang X, Chang Z, Xue M, Zhao Y, Meng X, Li B, Zhang X, Zhang D, Zhao X, Gao C, Li J, and Li C*. (2024). Peptide REF1 is a local wound signal promoting plant regeneration. Cell 187: https://doi.org/10.1016/j.cell.2024.04.040