Genome-Wide Analysis of the SlSIZ Gene Family in Tomato and the Role of SlSIZ1 and SlSIZ4 in Salt Stress Tolerance

Salinity is an abiotic constraint that limits the growth and productivity of tomato (Solanum lycopersicum L.). However, the role of small ubiquitin-like modifier (SUMO) E3 ligases (SIZs) in the salt stress response in tomato remains unknown. Here, a genome-wide analysis identified four SIZ-type genes in tomato, designated SlSIZ1–SlSIZ4. Gene structure and conserved motif analyses revealed the canonical SAP (SAF-A/B, Acinus, and PIAS) domain and the SP-RING (Siz/PIAS RING finger) domain in all SlSIZ proteins. Phylogenetic analysis grouped SIZ proteins from tomato and representative plant species into five major groups (A–E), with SlSIZ members distributed across distinct clades, and members within each clade shared conserved gene structures. Online transcriptome data and our qRT-PCR analyses showed that SlSIZ4 was highly expressed in leaves, flowers, and fruits, whereas SlSIZ1 showed broad expression, with relatively higher levels in roots, flowers, and multiple fruit stages. Under salt stress, abscisic acid (ABA), and methyl jasmonate (MeJA) treatments, the expression of SlSIZ1 and SlSIZ4 was strongly induced, whereas the expression of SlSIZ2 and SlSIZ3 was rarely promoted. In addition, virus-induced gene silencing (VIGS) of SlSIZ1 and SlSIZ4 markedly reduced salt tolerance of tomato seedlings, as reflected by growth inhibition, chlorophyll loss, increased reactive oxygen species (ROS), reduced proline accumulation, and diminished antioxidant gene expressions. Collectively, these findings identify SlSIZ1 and SlSIZ4 as positive regulators of salt stress tolerance in tomato and provide a framework for further dissection of the SlSIZ gene family.