A novel microRNA, SlymiR208, promotes leaf senescence via regulating cytokinin biosynthesis in tomato

Abstract

Leaf senescence is a highly‐programmed developmental process during the plant life cycle. Cytokinin (CK) has been widely acknowledged as a negative regulator to delay leaf senescence. MiRNAs play key roles in a variety of developmental and physiological processes through negatively regulating their target gene expression. However, to date, the roles of microRNAs (miRNAs) in CK biosynthesis remain unclear, and the knowledge on miRNA regulation of leaf senescence is still very limited. Isopentenyltransferases (IPTs) catalyze the initial and rate‐limiting step of CK biosynthesis in higher plants. Our previous work uncovered that silencing of SlIPT4 expression in tomato resulted in premature leaf senescence. Here, we identified a novel tomato miRNA, SlymiR208, which regulates the expression of SlIPT2 and SlIPT4 at the post‐transcriptional level. SlymiR208 expression is ubiquitous in tomato and exhibits an opposite transition to its target transcripts in aged leaf. SlymiR208 overexpression in tomato sharply reduced the transcript levels of SlIPT2 and SlIPT4, and the concentrations of endogenous CKs in leaves. The early leaf senescence caused by SlymiR208 overexpression was consistent with the phenotype of SlIPT4‐silenced lines. The data demonstrated that SlymiR208 is a positive regulator in leaf senescence through negatively regulating CK biosynthesis via targeting SlIPT2 and SlIPT4 in tomato. This study indicated that post‐transcriptional regulation via miRNA is a control point of CK biosynthesis and added a new layer to the understanding of the regulation of CK biosynthesis in tomato and a new factual proof to support that miRNAs are involved in leaf senescence.

New Advances in the Regulation of Leaf Senescence by Classical and Peptide Hormones

“…Overexpression of FPS1S (Farnesyl diphosphate synthase) leads to the declined endogenous zeatin-type CK with a concomitant senescence-like phenotype in Arabidopsis (Masferrer et al, 2002 ). SlymiRNA208 suppresses the post-transcriptional expression of SlIPT2 and SlIPT4 in tomato, resulting in the premature leaf senescence in the SlymiRNA208 -overexpressing plants by reducing the endogenous concentration of CKs (Zhang et al, 2020b ). APT1 (Adenine phosphoribosyl transferase 1), which catalyzes the CK conversion from free bases to nucleotides, acts as a positive regulator of leaf senescence.…”

Tomato MicroRNAs and Their Functions

“…Indeed, the ectopic expression of the sly-miR208 precursor ( 35S::pre-miR208 ) increased the levels of sly-miR208 and reduced the transcript levels of SlIPT2 and SlIPT4 in leaves. Moreover, RLM-RACE revealed that SlIPT2 and SlIPT4 encoding transcripts undergo sly-miR208-guided cleavage in the leaves of 35S::pre-miR208 plants, further supporting their targeting by this putative miRNA [ 101 ]. However, further research is required to confirm that SlIPT2 and SlIPT4 are negatively regulated by the endogenous sly-miR208 and to establish the biological significance of this regulation for cytokinin-mediated tomato development.…”

Multiple Layers of Regulation on Leaf Senescence: New Advances and Perspectives

“…miR398 participates in regulating leaf senescence by post-transcriptional regulation of ASCORBATE PEROXIDASE 6 ( APX6 ) ( Chen et al, 2021 ). SlymiR208 regulates leaf senescence by controlling the expression of isopentenyl transferases SlIPT2 and SlIPT4 ( Zhang Y. et al, 2020 ).…”