Differential Roles of Two Homologous Cyclin-Dependent Kinase Inhibitor Genes in Regulating Cell Cycle and Innate Immunity in Arabidopsis

Abstract

Precise cell-cycle control is critical for plant development and responses to pathogen invasion. Two homologous cyclindependent kinase inhibitor genes, SIAMESE (SIM) and SIM-RELATED 1 (SMR1), were recently shown to regulate Arabidopsis (Arabidopsis thaliana) defense based on phenotypes conferred by a sim smr1 double mutant. However, whether these two genes play differential roles in cell-cycle and defense control is unknown. In this report, we show that while acting synergistically to promote endoreplication, SIM and SMR1 play different roles in affecting the ploidy of trichome and leaf cells, respectively. In addition, we found that the smr1-1 mutant, but not sim-1, was more susceptible to a virulent Pseudomonas syringae strain, and this susceptibility could be rescued by activating salicylic acid (SA)-mediated defense. Consistent with these results, smr1-1 partially suppressed the dwarfism, high SA levels, and cell death phenotypes in acd6-1, a mutant used to gauge the change of defense levels. Thus, SMR1 functions partly through SA in defense control. The differential roles of SIM and SMR1 are due to differences in temporal and spatial expression of these two genes in Arabidopsis tissues and in response to P. syringae infection. In addition, flow-cytometry analysis of plants with altered SA signaling revealed that SA is necessary, but not sufficient, to change cell-cycle progression. We further found that a mutant with three CYCD3 genes disrupted also compromised disease resistance to P. syringae. Together, this study reveals differential roles of two homologous cyclin-dependent kinase inhibitors in regulating cell-cycle progression and innate immunity in Arabidopsis and provides insights into the importance of cell-cycle control during host-pathogen interactions.

Should I fight or should I grow now? The role of cytokinins in plant growth and immunity and in the growth–defence trade-off

“…Interestingly, perturbations of the cell cycle can lead to activation of plant immunity (Bao et al, 2013). Recently, two cell cycle CDK proteins, SIAMESE (SIM) and SIM-RELATED 1 (SMR1), were found to be essential for cell cycle control and proper activation of programmed cell death during ETI (Wang et al, 2014;Hamdoun et al, 2016). The activation of SIM and SMR1 is also dependent on the CPR5 gene, encoding a nuclear envelope protein, and whose mutations show constitutive activation of defence and growth defects.…”

Tissue-Specific Control of the Endocycle by the Anaphase Promoting Complex/Cyclosome Inhibitors UVI4 and DEL1

“…Endoreplication has also been demonstrated to instruct cell fate, as observed for Arabidopsis trichomes . More recently, endocycle modulators have been implicated in the control of innate immunity in Arabidopsis (Hamdoun et al, 2016), suggestive for the importance of the endocycle in the plant immunity.…”

Why do plants need so many cyclin-dependent kinase inhibitors?

“…redundancy in both CKI gene families, suggesting that divergence in biochemical function plays a minor role in maintaining the number of genes. 18,20,21 Of particular note, Kumar and coworkers found that 10 different SMRs, including an SMR from the bryophyte Physcomitrella patens, can complement the trichome cell division phenotype of Arabidopsis sim mutants. 13 Additionally, individual KRP and the SMR genes show distinct patterns of tissue-specific and stress-regulated expression, consistent with the individual genes playing roles in integrating the cell cycle with a wide variety of signals.…”

“…More recent work shows that smr1 mutants have increased pathogen susceptibility 21 and that both SMR1 and KRP2 play roles in Arabidopsis effector-triggered immunity to bacterial and fungal pathogens through a physical interaction with a nuclear envelope protein CONSTITUTIVE EXPRESSOR OF PATHO-GENESIS-RELATED GENES5 (CPR5), apparently by contributing to the hyperphosphorylation of the key cell cycle regulator RETI-NOBLASTOMA-RELATED1 (RBR1). 32 The observation that CKIs contribute to hyperphosphorylation of RBR1 is somewhat paradoxical in light of the evidence that SMRs and KRPs are wellcharacterized inhibitors of CDK kinase activity, as discussed above.…”