A SlCLV3-S1WUS module regulates auxin and ethylene homeostasis in low light-induced tomato flower abscission

Authors: CHENG, LINA - Shenyang Agricultural University; LI, RUIZHEN - Shenyang Agricultural University; WANG, XIAOYANG - Shenyang Agricultural University; GE, SIQI - Shenyang Agricultural University; WANG, SAI - Shenyang Agricultural University; LIU, XIANFENG - Shenyang Agricultural University; HE, JING - Shenyang Agricultural University; Jiang, Cai-Zhong; QI, MINGFANG - Shenyang Agricultural University; XU, TAO - Shenyang Agricultural University; LI, TAINLAI - Shenyang Agricultural University

Submitted to: The Plant Cell
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/3/2022
Publication Date: 8/16/2022
Citation: Cheng, L., Li, R., Wang, X., Ge, S., Wang, S., Liu, X., He, J., Jiang, C., Qi, M., Xu, T., Li, T. 2022. A SlCLV3-S1WUS module regulates auxin and ethylene homeostasis in low light-induced tomato flower abscission. The Plant Cell. 34:4388-4408. https://doi.org/10.1093/plcell/koac254.
DOI: https://doi.org/10.1093/plcell/koac254

Interpretive Summary: Abscission of vegetative or reproductive organs occurs in the abscission zone at specific positions of plant, and is triggered by developmental and environmental cues. Organ abscission often occurs under low light stress and can result in substantial yield loss. Plant responses to light stress are associated with altered auxin and ethylene signaling pathways that regulate abscission processes. The continuous polar flow of auxin passing through the AZ inhibits abscission whereas impaired auxin transport or depletion in the AZ induces abscission initiation due to enhanced sensitivity of the AZ to ethylene. However, the molecular mechanisms involved in AZ responses to low light stress, and the basis of their integration into ethylene and auxin signaling systems remain unknown. It has been demonstrated that peptide signals are widely involved in organ abscission induced by environmental stimuli. In Arabidopsis thaliana, one example is the IDA-HAE/HSL2 module, which is associated with drought-induced leaf abscission. In tomato, phytosulfokine (PSK) and IDL6 were found to be involved in stress-induced flower pedicel abscission. However, these small peptides are thought to be involved in abscission by regulating the gene expression related to cell wall hydrolases, and not depending on the ethylene and auxin pathways. Another well characterized group of peptide hormones are members of the CLE (CLAVATA3/Embryo surrounding region-related) gene family. A classic feedback system, including the WUS (WUSCHEL) homeodomain transcription factor and CLV3 peptide, provides the basis for maintaining stem cell populations in the shoot apex meristem. In Arabidopsis, WUSCHEL-LIKE HOMEOBOX13 (WOX13) transcription factor negatively regulates fruit dehiscence and alters the gene expression associated with cell separation at the valve margin. CLE peptides have been reported to act as key signals in response to environmental stimuli and to mediate hormone homeostasis. A recent study showed that light regulates meristem activity by activating cytokinin signaling and inhibiting CLV3 and CLV1 expression in Arabidopsis. Moreover, the CLE genes were reported to be expressed in the AZ of Arabidopsis floral organ. However, whether CLE signals play a role in the abscission process remains to be elucidated. Here, we found that a gene encoded CLAVATA3 (CLV3), a peptide hormone that regulates stem cell fate in meristems was highly expressed in tomato pedicel abscission zone in response to low light treatment (shading). CRISPR-Cas9-mediated SlCLV3 knockout lines showed significantly delayed low light-induced flower drop. We also observed that the CLV3 signal depended on the receptor kinases CLV1 and BAM1 to reduce the expression of the WUSCHEL (WUS) transcription factor in the abscission zone. The delayed abscission phenotype in the CRISPR/cas9 CR-slclv3 mutant plants could be rescued by silencing WUS in the abscission zone. Using DNA affinity purification sequencing, transcription factors KD1 and FUL2 were identified as WUS target genes. Our data also demonstrated that low light stress reduced the expression of WUS and caused increased KD1 and FUL2 expression in the AZ, thereby perturbing the auxin response gradient and causing increased ethylene production, resulting in abscission initiation. Our results suggest that the CLV-WUS signaling pathway plays a central role in low light-induced abscission by affecting auxin and ethylene homeostasis.

Technical Abstract: The premature abscission of flowers and fruits due to environmental stress can seriously affect crop yields. However, the molecular mechanisms that regulate organ abscission in responses to low light stress are still unknown. Here, we found that a gene encoded CLAVATA3 (CLV3), a peptide hormone that regulates stem cell fate in meristems was highly expressed in tomato pedicel abscission zone in response to low light treatment (shading). CRISPR-Cas9-mediated SlCLV3 knockout lines showed significantly delayed low light-induced flower drop. We also observed that the CLV3 signal depended on the receptor kinases CLV1 and BAM1 to reduce the expression of the WUSCHEL (WUS) transcription factor in the abscission zone. The delayed abscission phenotype in the CRISPR/cas9 CR-slclv3 mutant plants could be rescued by silencing WUS in the abscission zone. Using DNA affinity purification sequencing, transcription factors KD1 and FUL2 were identified as WUS target genes. Our data also demonstrated that low light stress reduced the expression of WUS and caused increased KD1 and FUL2 expression in the AZ, thereby perturbing the auxin response gradient and causing increased ethylene production, resulting in abscission initiation. Our results suggest that the CLV-WUS signaling pathway plays a central role in low light-induced abscission by affecting auxin and ethylene homeostasis.