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. 2021 May 14;16(9):1928819. doi: 10.1080/15592324.2021.1928819

Ammonium-mediated reduction in salicylic acid content and recovery of plant growth in Arabidopsis siz1 mutants is modulated by NDR1 and NPR1

Ju Yong Kim a, Jong Tae Song b, Hak Soo Seo a,c,✉
PMCID: PMC8281091  PMID: 33989128

ABSTRACT

The siz1 mutants exhibit high SA accumulation and consequently severe dwarfism. Although siz1 mutants exhibit growth recovery upon exogenous ammonium supply, the underlying mechanism remains unknown. Here, we investigated the effect of ammonium on SA level and plant growth in SA-accumulating mutants. The growth of siz1-2 and siz1-3 mutants was recovered to wild-type (WT) levels upon exogenous ammonium supply, but that of siz1-3 ndr1 (non-race-specific disease resistance 1) and siz1-3 npr1 (non-expressor of pathogenesis related gene 1) double mutants was unaffected. The SA level was decreased by exogenous ammonium application in siz1-3 ndr1, siz1-3 npr1, and siz1-3 mutants. The level of nitrate reductase (NR) was almost the same in all genotypes (WT, siz1-3, ndr1, npr1, siz1-3 ndr1, and siz1-3 npr1), regardless of the ammonium treatment, suggesting that exogenous ammonium supply to ndr1 siz1-3 and npr1 siz1-3 double mutants does not have any effect on their growth and NR levels, but decreases the SA level. Taken together, these results indicate that ammonium acts as a signaling molecule to regulate the SA amount, and NDR1 and NPR1 play a positive role in the ammonium-mediated growth recovery of siz1 mutants.

KEYWORDS: Ammonium, AtSIZ1, nitrate reductase, salicylic acid, ndr1, npr1

Introduction

Salicylic acid (SA) is a plant hormone that mediates host defense response and is upregulated upon pathogen infection. Plants overexpressing NahG, encoding a salicylate hydroxylase that degrades SA, are unable to accumulate SA upon pathogen infection1. SA is synthesized via the isochorismate synthase (ICS) or phenylalanine ammonia-lyase (PAL) pathway, depending on the plant species.2 For example, the ICS pathway is important for SA biosynthesis in Arabidopsis thaliana, whereas the PAL pathway seems to be more important for SA accumulation in rice (Oryza sativa L.). In soybean (Glycine max L.), both pathways contribute equally to SA accumulation. SA can undergo various modifications such as the addition of a glucose molecule, methyl group, hydroxyl group, and an amino acid. In most cases, SA modifications result in its inactivation or catabolism.3–6

E3 SUMO ligase mediates the covalent conjugation of small ubiquitin-related modifier (SUMO) to a lysine residue of target proteins. Arabidopsis E3 SUMO ligase AtSIZ1, an SP-RING finger protein harboring a DNA-binding SAP domain and zinc finger Miz domain, is involved in seed germination,7,8 flowering,9,10 epigenetic regulation,11,12 nutrient utilization,13,14 and stress response.15,16 The siz1 mutants display small leaves and severe dwarfism,17 but revert to the wild-type (WT) phenotype when treated with exogenous ammonium.13

Ammonium is a major inorganic nitrogen source for plants. Low levels of external ammonium promote plant growth,18 but high levels cause toxicity.19 Several studies have shown that ammonium triggers multiple physiological and morphological responses through specific changes in gene expression, metabolism, redox status, and root system architecture.20–23 Many of these responses including root growth inhibition, lateral root branching, starvation-induced uptake of ammonium, and its toxicity are independent of ammonium assimilation, implying that ammonium acts as a signaling molecule.

The siz1–3 single mutant and siz1–3 ndr1 and siz1–3 npr1 double mutants exhibit a dwarf phenotype.13,24 Additionally, the siz1–3 and siz1–3 npr1 mutants accumulate SA to high levels.13,24 However, in the siz1–3 mutant, the high SA amount decreases to the WT level by ammonium treatment.13 These data suggest that ammonium treatment affects the growth and SA content of siz1–3 ndr1 and siz1–3 npr1 double mutants. In this study, we investigated the effect of exogenous ammonium treatment on the growth and SA content of siz1–3 ndr1 and siz1–3 npr1 double mutants. The results showed that exogenous ammonium supply decreased the SA levels in siz1–3 ndr1, siz1–3 npr1, and siz1–3 mutants to WT levels but had no effect on their growth.

Materials and methods

Plant material and culture conditions

Arabidopsis thaliana ecotype Columbia-0 (Col-0; WT) and siz1–2, siz1–3, ndr1, npr1, siz1–3 ndr1, and siz1–3 npr1 mutants were used in this study. Plants were grown in fully automated growth chambers at 22°C day/20°C night temperature under a 16 h light/8 h dark photoperiod either on 0.75% agar media containing Murashige and Skoog (MS) salts, 0.5 g/l MES, and 10 g/l sucrose, or in soil (a mixture of vermiculite and perlite (1 : 1 mixture)). To investigate the effect of different nitrogen sources, WT and mutant seeds were germinated and grown on MS-agar media. After 4 days, seedlings were transplanted into soil and fertilized every 5 d with a solution containing 5 mM K2SO4, KNO3, or (NH4)2SO4. All experiments were repeated three times, unless stated otherwise.

Examination of nitrate reductase (NR) level

WT, siz1–3, ndr1, npr1, siz1–3 ndr1, and siz1–3 npr1 plants were grown for 15 days in MS media and then treated with 5 mM K2SO4, KNO3 or (NH4)2SO4 for 8 h. Total protein extract was prepared from the leaves of each genotype and separated by sodium dodecyl sulfate-polyacrylamide gel electrophoresis (SDS-PAGE) on 8% acrylamide gels. The levels of NRs, NIA1 and NIA2, were examined by western blot analysis with cucumber anti-NR antibody (antibodies-Online).

Determination of SA content

Shoots of 4-week-old plants grown in soil under long-day conditions with or without 20 mM (NH4)2SO4 were harvested and ground to a fine powder in liquid nitrogen. One gram of powdered tissue was extracted in 10 mL of 100% methanol at 4°8 hours)C for 24 h. Then, 6 mL of water and 5 mL of chloroform were added to each sample and vortexed. The samples were then stored at 4°C for 24 h. Supernatants were dried under nitrogen gas. The pellets were resuspended in 1 mL of 70% methanol, and SA was quantified by high performance liquid chromatography (HPLC), as described previously.25

Results

We reported previously that the phenotypes of Arabidopsis siz1–2 mutants reverted to the WT phenotype upon treatment with exogenous ammonium, but not with nitrate, phosphate, or potassium, during the reproductive and vegetative growth phases.13 The ndr1 and npr1 mutants did not exhibit an increase in PR1 protein26 and did not accumulate SA,24 whereas the siz1–2 mutant accumulated the PR1 protein as well as SA to high levels.13 Additionally, Arabidopsis siz1–3 ndr1 and siz1–3 npr1 double mutants exhibited dwarf phenotypes24 (Figure 1), suggesting that the phenotype of these double mutants is affected by ammonium as the nitrogen source. Therefore, in this study, we examined the effect of ammonium on the growth of ndr1, npr1, siz1–3 ndr1, and siz1–3 npr1 mutants as well as on WT, siz1–2, and siz1–3 plants, which served as controls. The results showed that siz1–2 and siz1–3 mutants recovered their phenotypes to the WT level when treated with exogenous ammonium but not when treated with nitrate (Figure 1). On the other hand, the phenotypes of siz1–3 ndr1 and siz1–3 npr1 double mutants were neither affected by exogenous ammonium nor by exogenous nitrate application (Figure 1). The growth of WT, ndr1, and npr1 plants was slightly stimulated by ammonium supply, indicating the effect of ammonium as a nutrient.

Figure 1.

Figure 1.

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Growth patterns of wild-type (WT) and mutant plants, and the effect of nitrogen sources on their growth. After germination on Murashige and Skoog (MS) media, seedlings were transferred to soil and treated with 5 mM K2SO4, KNO3, or (NH4)2SO4 for 15 or 30 d

Previously, we showed that the dwarf phenotype of the siz1–2 mutant was associated with low NR activity and stability and high SA level.13 Therefore, we speculated that the dwarf phenotypes of siz1–3 ndr1 and siz1–3 npr1 double mutants were caused by low levels of NRs (NIA1 and NIA2) and high SA amount. To test this possibility, we first examined the level of NIA1 and NIA2 proteins in ndr1, npr1, siz1–3 ndr1, and siz1–3 npr1 plants by immunoblotting with cucumber anti-NR antibody, which cross-reacts with both NIA1 and NIA2. Levels of both NIA1 and NIA2 were almost the same across all genotypes not treated with exogenous ammonium (Figure 2). Similar results were obtained in plants treated with ammonium (Figure 2). Moreover, NIA1 and NIA2 levels did not change in samples treated with K2SO4 (control) (Figure 2). These results suggest that NDR1 and NPR1 are not required to regulate the level of NRs. Nonetheless, this does not exclude the possibility that the activity of NRs can be modulated by NDR1 and NPR1.

Figure 2.

Figure 2.

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Examination of nitrate reductase (NR) levels in WT and mutant plants. WT, siz1–3, ndr1, npr1, siz1–3 ndr1, and siz1–3 npr1 plants were grown in soil under long-day conditions. Total proteins were extracted, and NIA1 and NIA2 proteins were detected by western blot analysis with cucumber anti-NR antibody. The anti-NR antibody was stripped, and the western blot was re-probed with anti-tubulin antibody

Next, we measured the SA level in ndr1, npr1, siz1–3 ndr1, and siz1–3 npr1 plants. SA was extracted from the leaves of plants treated with or without (NH4)2SO4 and analyzed by HPLC as described by Freeman et al. (2005).25 Compared with the WT, the SA level was almost the same in ndr1 but slightly higher in the npr1 mutant (Figure 3). In the exogenous ammonium treatment, SA levels in ndr1 and npr1 mutants were decreased to the level found in the WT (Figure 3). SA levels in siz1–3 siz1–3 ndr1 mutants and particularly in the siz1–3 npr1 mutant were much higher than that in the WT. Interestingly, SA levels in ammonium-treated siz1–3, siz1–3 ndr1, and siz1–3 npr1 plants also decreased to the level in the WT (Figure 3), although their growth did not recover to the WT level (Figure 1).

Figure 3.

Figure 3.

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Effect of ammonium source on SA levels in WT and mutant plants. WT, siz1–3, ndr1, npr1, siz1–3 ndr1, and siz1–3 npr1 plants were grown in soil containing 5 mM K2SO4 or (NH4)2SO4 under long-day conditions. SA were extracted and detected by high performance liquid chromatography (HPLC). The free SA values ± standard error are averages of five replicates of samples. The number of asterisks indicates samples that are different from one another at a given level (**P < .01; ***P < .001, t-tests). Ammonium-treated and – untreated WTs were not significantly (NS) different for SA level (P > .5, t-test)

Discussion

SA has growth-stimulating effects in soybean, wheat, maize, and chamomile.27–30 However, in Arabidopsis, SA has a negative effect on plant growth. For example, Arabidopsis plants overexpressing OBP3, which encodes an SA-inducible DOF (DNA-binding with one finger) transcription factor, exhibit reduced growth rate or death.31 Similar results have also been reported in the SA-accumulating mutants such as cpr5 (constitutive expressor of PR5), acd6–1 (accelerated cell death 6–1), and agd2 (aberrant growth and death 2).32–34 By contrast, the SA-depleted Arabidopsis NahG transgenic plants exhibit higher growth rate.35

In this study, we showed that SA levels were higher in siz1–3 ndr1 and siz1–3 npr1 double mutants than in the WT (Figure 3), but decreased to WT levels upon exogenous ammonium application (Figures 3 and 4). Nevertheless, the growth of siz1–3 ndr1 and siz1–3 npr1 mutants did not recover following exogenous ammonium treatment (Figures 1 and 4). These results suggest that growth inhibition in Arabidopsis is regulated not only by SA content but also by the interaction of SA signaling with other signaling pathways, indicating the involvement of components controlling SA signaling such as NDR1 and NPR1.

Figure 4.

Figure 4.

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Schematic representation of the regulation of SA content and growth by ammonium. (a) SA level in ammonium-treated siz1 mutants decreased to the level in the WT and they recovered their phenotypes to the WT level. (b) SA level in ammonium-treated siz1 ndr1 or siz1 npr1 double mutants decreased to the level in the WT. But, their growth did not recover to the WT level. (c) Infection of plants with Pseudomonas syringae pv. phaseolicola accumulated SA when treated with nitrate while SA levels were decreased when treated with ammonium.36

Compared with the siz1–3 mutant, the SA amount was approximately 2-fold lower in the siz1–3 ndr1 double mutant and approximately 2-fold higher in siz1–3 npr1 (Figure 3). These results suggest that NDR1 and NPR1 have different effects on the regulation of SA amount increased by AtSIZ1 loss, positive and negative effects of NDR1 and NPR1, respectively.

The ndr1 mutant did not accumulate SA, while the npr1 mutant accumulated SA to a slightly higher level than the WT24,37 (Figure 3). Phenotypes of both ndr1 and npr1 mutants were similar to that of the WT24 (Figure 1). However, siz1–3 ndr1 and siz1–3 npr1 double mutants displayed dwarf phenotypes, similar to the siz1–3 mutant, although the SA level was lower in siz1–3 ndr1 and higher in siz1–3 npr1 compared with the siz1–3 mutant. These results suggest that AtSIZ1 is epistatic to NDR1 and NPR1; thus the exogenous ammonium application has no effect on the level of NRs, NIA1 and NIA2, in siz1–3 ndr1 and siz1–3 npr1 double mutants.

NDR1 is a plasma membrane protein and plays an important role in electrolyte release in response to bacterial pathogen infection as well as in the maintenance of plasma membrane–cell wall junction.38 NPR1 is a cytosolic protein that acts as an SA receptor and controls plant immunity by inducing target gene expression as a transcriptional coregulator.39–41 Therefore, we carefully infer that NDR1-mediated electrolyte release and NPR1-mediated transcriptional regulation are involved in AtSIZ1-mediated SA signaling and plant growth.

Gupta et al. (2013) showed that nitrate-treated plants accumulated more SA and less PR1a expression than ammonium-treated plants after pathogen inoculation (Figure 4), indicating that ammonium supply suppresses SA accumulation.

In conclusion, our data indicate that ammonium acts as a signaling molecule to negatively regulate the SA amount, and AtSIZ1-mediated plant growth is affected by the functions of SA signaling proteins NDR1 and NPR1.

Acknowledgments

This work was carried out with the support of “Cooperative Research Program for Agriculture Science and Technology Development (Project No. PJ01567701)” Rural Development Administration, Republic of Korea.

Funding Statement

This work was supported by the Cooperative Research Program for Agriculture Science and Technology Development (Project, Rural Development Administration [PJ01567701].

Disclosure statement

The authors report no conflict of interest.

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