Rice seed germination priming by salicylic acid and the emerging role of phytohormones in anaerobic germination

Abstract

Direct seeding has been increasingly adopted under both rainfed and irrigated conditions due to its low cost and convenience. Not only to suppress weed germination and reduce the cost of manual weeding and/or dependence on herbicides, but also to control pests and reduce pesticide usage, farmers usually flood the direct-seeded field, resulting in inadequate seed germination and seedling establishment (Ismail et al., 2012). It is crucial to develop rice varieties with tolerance to submerged conditions for successful seed germination for the widespread adoption of direct seeding (Hsu and Tung, 2015). Hence, elucidating the mechanism of submerged germination in rice is a key scientific issue. The biosynthesis, catabolism, and modification of phytohormones such as abscisic acid (ABA), gibberellin (GA), jasmonic acid (JA), and auxin (indole-acetic acid: IAA) are critical for seed germination and coleoptile elongation under submergence in rice (He et al., 2023; Lee et al., 2023; Sun et al., 2022; Wang et al., 2024). Among these, excessive IAA accumulation will cause poor anaerobic germination in rice, suggesting that a certain threshold level of IAA is essential for rice submergence tolerance (Lee et al., 2023). GA is suggested to promote submerged germination, which is based on the decreased performance of GA 20-oxidase gene (OsGA20ox1) knockout lines (Sun et al., 2022). Whether exogenously applied GA promotes rice submerged germination remains unknown. Salicylic acid (SA) is a key plant hormone in plant immunity (Ding and Ding, 2020). Whether SA is involved in seed germination under submerged conditions is poorly understood in plants. A recent study by Wang et al. (2024) discovered that SA positively regulates submerged germination by affecting IAA catabolism in rice. This study provides new insights into the mechanisms of SA as a promoter of submerged germination in rice. Thus, SA is likely the only phytohormone that can be used in rice seed priming to promote submerged germination. Till now, several studies have found that the interaction between different hormone functions play a critical role in ensuring seed germination under submerged conditions (Figure 1). First, the rice 14-3-3 protein-coding gene OsGF14h acts as a signal switch to inhibit ABA signaling by interacting with the transcription factors homeobox 3 (OsHOX3) and viviparous 1 (OsVP1), and to increase GA synthesis, thereby enhancing submerged germination and seedling development (Sun et al., 2022). Second, the rice UDP-glucosyltransferase OsUGT75A can glycosylate ABA and JA, thereby reducing both free ABA and JA levels and promoting submerged germination and coleoptile growth (He et al., 2023). Thus, the crosstalk between ABA and JA signaling and the balance between ABA signaling and GA biosynthesis function in submergence tolerance during rice seed germination. Interestingly, in a recent study, Wang et al. (2024) uncovered the crosstalk of SA and IAA functions in rice submerged germination. Wang et al. (2024) found the peroxisomal CA-coenzyme A (CoA) ligases (OsCNL1/2), which are involved in the biosynthesis of SA, are highly induced during submerged imbibition. They reported that the high accumulation of SA is essential for submerged germination; SA promotes IAA catabolism through multiple Gretchen Hagen 3 (GH3)-dependent IAA-amino acid conjugation, thereby removing IAA inhibition of germination (Wang et al., 2024). The results of these recent studies significantly elucidated the phytohormones regulatory network in rice submerged germination. Crosstalk of hormone signaling pathways regulates rice submerged germination (based on Sun et al., 2022; He et al., 2023; Wang et al., 2024) First, the balance between abscisic acid (ABA) signaling and the gibberellin (GA) biosynthesis pathway regulates submerged germination, which is mediated by Oryza sativa 14-3-3 protein-coding gene (OsGF14h). OsGF14h acts as an ABA signaling switch which activates a transcriptional repressor O. sativa homeobox transcription factor (OsHOX3) and inhibits a transcriptional activator O. sativa viviparous1 (OsVP1). Meanwhile, OsGF14h and OsHOX3 can transactivate unknown downstream genes to promote GA biosynthesis, resulting in the inhibition of ABA-responsive genes to promote submerged germination (Sun et al., 2022). Second, the crosstalk of jasmonic acid (JA) and ABA signaling pathways regulates submerged germination, which is regulated by O. sativa UDP-glucosyltransferase 75A (OsUGT75A). OsUGT75A catalyzes the glycosylation of ABA and JA, which contributes to the reduction of free ABA and JA accumulation, leading to the inhibition of ABA signaling to promote submerged germination (He et al., 2023). Third, crosstalk between salicylic acid (SA) and indole-acetic acid (IAA) metabolism regulates rice submerged germination, which is triggered by the expression of OsCNLs. O. sativa cinnamate: CoA ligases (OsCNLs) undertake SA biosynthesis to induce O. sativa Gretchen Hagen 3 (OsGH3)-mediated IAA-amino acid conjugation, thereby releasing the inhibition of rice submerged germination by IAA (Wang et al., 2024). Usually, the japonica accessions have better submerged germination than the indica (Hsu and Tung, 2015; He et al., 2023). The details of the underlying mechanism have been elucidated to some extent. Submergence tolerance is associated with natural variation in the calcineurin B-like protein 10 (OsCBL10) promoter region, and the tolerant type of promoter is only present in japonica cultivars (Ye et al., 2018). The elite allele of OsUGT75A, which is associated with enhanced submerged germination, is mainly found in japonica accessions (He et al., 2023). These are the potential target genes for breeding varieties with submergence tolerance using marker-assisted selection and/or transgenic approaches. However, the current process of rice breeding is limited by the lack of functional genes, low efficiency and high cost. Interestingly, the work of Wang et al. (2024) developed the strategies to improve rice submerged germination by SA pretreatment with the advantages of high efficiency and low cost. This work showed that imbibing rice seeds with 500 µmol/L SA for 24 h significantly increased submerged germination and seedling establishment in both japonica and indica varieties. More importantly, the cost of SA pretreatment is about 0.4–0.6 yuan per hectare, indicating the feasibility of SA pretreatment for direct seeding of rice (Wang et al., 2024). Thus, SA pretreatment appears to be a promising method for improving submerged germination of rice for direct seeding. The key message from the study by Wang et al. (2024) is that SA promotes submerged germination via OsGH3-mediated IAA catabolism and that SA pretreatment is a cost-effective strategy to improve submerged germination in rice. However, there are some questions that need to be investigated in the future regarding the effect of SA on submergence tolerance. For example, what are the mechanisms of GH3 gene induction by SA, what specific factors regulate OsCNL1/2 expression induction during submerged germination, and is OsCNL1/2 the potential target gene for breeding varieties? Seed priming is a pre-sowing treatment in which seeds are partially hydrated to a level that prevents radical emergence. It has long been studied as an effective technique to achieve enhanced germination, better synchronicity, improved seedling vigor, and hence greater resistance to environmental stresses (Bera et al., 2022). The primed seeds could be stored for a long time for the next season's sowing. How effectively can SA be used as a priming agent to improve submerged germination in rice cultivation practice? Overall, addressing these questions will deepen our understanding of SA in improving of submergence tolerance for direct seeding in crops. What is more, direct seeding of rice is subject to high lodging, while deep seeding can effectively increase lodging tolerance (Lee et al., 2017). Thus, increased seedling emergence under deep seeding field condition is particularly critical for mechanical direct seeding. Interestingly, Wang et al. (2024) observed that covering cnl1 cnl2 seeds with sand can further and strongly exacerbate the delayed germination phenotype. Further investigation is needed to understand whether CNL regulates seed germination under deep sowing conditions during direct seeding of rice. As OsGH3-2 is known to be associated with seed storability and seed vigor in rice (Yuan et al., 2021). It will be interesting to investigate whether CNL and SA have functions in seed storability. It is noteworthy that IAA controls seed dormancy by stimulating ABA signaling (Liu et al., 2013). Therefore, it will be worthwhile to investigate whether CNL and SA can modulate seed dormancy in crop plants. Ultimately, further elucidating the role of SA in seedling establishment, seed storability, and even seed dormancy will help us to develop varieties with high seed vigor for direct seeding and ensure crop yield. This work was supported by National Natural Science Foundation of China (32372156, 32172052, 32272157, and 32201838) and the Natural Science Foundation of Guangdong Province (2023A1515012092 and 2023A1515012052). The authors declare no conflict of interest. Z.W. conceptualized the idea; Y.H. and J.Z. wrote the initial draft and prepared the figure. All authors have read and approved the final version of the manuscript.

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