Soil salinization has emerged as a major environmental challenge that threatens agriculture across the world due to the fact that approximately 20% of the world’s irrigated agricultural lands are salt-affected (Hazell and Wood, 2008; Qadir et al., 2014; Gong et al., 2020; Zhao et al., 2021). Rice (Oryza sativa L.) is one of the most salt-sensitive cereal crops and is highly sensitive at the early seedling stage, and salt stress induces both toxicity and osmotic stress, resulting in growth inhibition, developmental changes, metabolic adaptations, and ion sequestration or exclusion in rice (Munns and Tester, 2008; Zelm et al., 2020; Wang et al., 2021). Salt response and tolerance in rice is a complicated process controlled by multiple genes and pathways (Zhao et al., 2021; Chen et al., 2022). Breeding salt-tolerant rice varieties will greatly contribute to the world’s food security but remains a great challenge.

Mitogen-activated protein kinase (MAPK/MPK) cascades play key roles in the signal perception and transduction of salt stress signaling in plants by transducing extracellular stimuli through sequential phosphorylation, and then phosphorylating substrates and modifying their activities (Gao et al., 2010; Chen et al., 2021). The rice genome contains 17 MAPK, 8 MAPKK, and 75 MAPKKK coding genes (Hamel et al., 2006; Jia et al., 2016). Recently, several MPK cascades mediating the rice salt response have been identified. OsMKK1, whose kinase activity was induced by salinity, positively regulated rice salt tolerance via activation of the downstream substrate OsMAPK4 (also known as OsMPK6) (Wang et al., 2014). OsMAPKKK63 is associated with OsMKK1 to enhance rice resistance to salt stress (Na et al., 2019). Overexpression of constitutively activated OsMPKK6 enhanced rice salt tolerance, and OsMPK3 and OsMPK6 were activated in salt stress response (Xiong and Yang, 2003; Xie et al., 2012; Kumar and Sinha, 2013). The kinase activity of OsMPK6 was upregulated by OsMKK4 in response to various stresses (Shen et al., 2010). OsMAPK3 showed a positive effect on salt tolerance by attenuating the reactive oxygen species accumulation (Zhang et al., 2018). Although different MPK cascades were shown to regulate salt response in rice, the substrates phosphorylated by MAPK during rice salt tolerance remain largely unknown.

The Ideal Plant Architecture 1 (IPA1) gene, encoding a SQUAMOSA promoter binding protein-like (SPL) transcription factor OsSPL14, has been reported to regulate rice plant architecture and substantially increase rice grain yield (Jiao et al., 2010; Miura et al., 2010; Wang et al., 2018a). In addition, IPA1 also regulates biotic and abiotic resistance. Overexpression of IPA1 enhanced disease resistance against bacterial blight caused by Xanthomonas oryzae pv. oryzae (Xoo) (Liu et al., 2019), and phosphorylated IPA1 could bind to the promoter of pathogen defense gene WRKY45 to activate its expression, leading to enhanced disease resistance against Magnaporthe oryzae (Wang et al., 2018b). IPA1 could improve rice drought tolerance at the seedling stage through the ABA pathway (Zhu et al., 2022). IPA1 has been broadly used in high-yield rice breeding and recognized as a new “Green Revolution” gene (Wang and Wang, 2017). Besides, other members of rice SPL also play important roles in growth and development (Unte et al. 2003; Xie et al., 2006), and some of them are related to abiotic stress tolerance. OsSPL10 negatively controls salt tolerance in rice (Lan et al., 2019). Downregulation of OsSPL13 enables the plant to survive better than wild type under drought conditions (Jerome Jeyakumar et al., 2020). However, whether and how IPA1 is involved in rice salt tolerance remains elusive.

In this study, we found that IPA1 could negatively regulate rice salt tolerance. Under salt stress, OsMPK4 (also known as OsMAPK7) could interact with and phosphorylate IPA1, leading to the degradation of IPA1. Biochemical and genetic analyses demonstrated that IPA1 acted as the downstream substrate of OsMPK4 to mediate rice salt tolerance. The OsMPK4-IPA1 module illustrated crosstalk between salt stress and development in rice, which will benefit breeding high-yield and salt-tolerant varieties in rice.