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Light signaling regulates root-knot nematode infection and development via HY5-SWEET signaling

BMC Plant Biology volume 24, Article number: 664 (2024) Cite this article

Abstract

Background

Meloidogyne incognita is one of the most important plant-parasitic nematodes and causes tremendous losses to the agricultural economy. Light is an important living factor for plants and pathogenic organisms, and sufficient light promotes root-knot nematode infection, but the underlying mechanism is still unclear.

Results

Expression level and genetic analyses revealed that the photoreceptor genes PHY, CRY, and PHOT have a negative impact on nematode infection. Interestingly, ELONGATED HYPOCOTYL5 (HY5), a downstream gene involved in the regulation of light signaling, is associated with photoreceptor-mediated negative regulation of root-knot nematode resistance. ChIP and yeast one-hybrid assays supported that HY5 participates in plant-to-root-knot nematode responses by directly binding to the SWEET negative regulatory factors involved in root-knot nematode resistance.

Conclusions

This study elucidates the important role of light signaling pathways in plant resistance to nematodes, providing a new perspective for RKN resistance research.

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Background

Outbreaks of plant-parasitic nematodes can cause severe economic losses, estimated at $77 - $157 billion each year [1]. Root-knot nematodes (RKNs, Meloidogyne spp.) are among the most widespread and damaging plant-parasitic nematodes worldwide. They can infect more than 5500 hosts, including crops, vegetables and fruits [2]. Three species of “tropical” root knot nematodes, Meloidogyne incognita, Meloidogyne javanica and Meloidogyne arenaria, are among the most rapidly spreading crop pests and pathogens [3]. One of the most important species is M. incognita, which causes damage to the global agricultural economy [4].

Light affects seed germination, circadian rhythms, flowering development and shade avoidance. These responses are mediated by several classes of photoreceptors, which absorb light of different wavelengths [5]. The main photoreceptors include phytochrome, which absorbs red and far-red light, and cryptochrome and phototropin, which absorb blue light. Photoreceptors play important roles in the interaction between the host and pathogen [6]. Compared with exposure to white light, cucumber exposure to red light resulted in higher levels of H2O2 and salicylic acid (SA) and stronger expression of defense genes such as PR-1. Therefore, red light enhances salicylic acid pathway-mediated resistance in cucumber [7]. In addition, red light treatment improves tomato resistance to Pseudomonas syringae [8]. Under blue light, CRY2/PHOT2 negatively regulates the proteasome-mediated degradation of HRT, likely via COP1, and blue light relieves this repression, resulting in HRT degradation, making plants resistant to turnip crinkle virus (TCV) [9]. The blue photoreceptor CRY1 has been identified in plants. The expression of the salicylic acid (SA)-induced pathogenesis-related gene PR-1 is reduced in cry1 mutants but is enhanced in cry1-ox plants. Therefore, the blue light photoreceptor CRY1 positively regulates inducible resistance to P. syringae [10].

Photoreceptors activate many intermediary transcription factors after absorbing different wavelengths, and several transcription factors that act downstream of either single or multiple photoreceptors have been functionally characterized [11, 12]. Among them, ELONGATED HYPOCOTYL5 (HY5) is a member of the basic-region leucine zipper (bZIP) family of transcription factors [13] and is involved in photomorphogenesis downstream of phytochromes, cryptochromes and photoreceptors [14]. In recent years, the functions of HY5 have been linked to the plant defense response signaling pathway. HY5/HYH directly bind to the promoters of the reactive oxygen species (ROS) signal-related genes APX2, ZAT10, SIB1, ERF4 and NDB2 [15]. Enhanced disease susceptibility 1 (EDS1) is a positive regulator of the basal resistance of plants to biological stress. HY5 enhances EDS1 expression by binding to the G-box of the EDS1 promoter and regulating the defense response in plants [16]. The plant hormone auxin (IAA) regulates plant disease responses. HY5 binds to the promoters of SLR and AXR2, which are negative regulators of auxin signaling, thereby regulating plant resistance to pathogens [17]. Brassinosteroids (BRs) play important roles in plant stress resistance, and HY5/HYH can directly bind to the promoter region of MSBP1 to inhibit BR synthesis [18]. HY5 affects both sucrose metabolism and shoot‒root transport by promoting the expression of TPS1, a gene encoding trehalose-6-phosphate synthase, and SWEET11 and SWEET12, genes encoding sucrose efflux transporters [19].

Light signaling plays an important role in pathogen infection and development. HY5, a core transcription factor involved in light signaling, has been extensively studied with respect to plant physiology. However, its involvement in the infection and development of plant-parasitic nematodes has not been reported. In this study, we revealed the mechanism through which photoreceptors, HY5, and SWEETs jointly influence RKN infection and development.

Methods

Plant material and growth conditions

Seeds for the phya-211, phyb-9, phya/b, cry1/2, phot1/2, cry1/2 phot1/2, hy5, pHY5:HY5-GFP hy5, sweet11a, sweet12b, sweet15d and sweet11a12b15d lines were obtained from the Carnegie Institution for Science. All the mutants were generated in the Col-0 background. Col-0 was used as the wild-type control. Seeds were vernalized at 4 °C for 72 h and germinated in plastic Ray Leach containers (4 cm in diameter and 13.5 cm high) containing equal ratios of sterilized sand and potting substrate (pH: 6.5–6.8; N, P, K ≥ 12 g/kg; water content ≤ 40%; organic content ≥ 40%; Si ≥ 0.3 g/kg) under the conditions of a 16-h/8-h photophase, 23–26 °C, and 50% relative humidity.

For light treatment, Arabidopsis (Col-0) seedlings were grown under white light (400–720 nm, 200 µmol m− 2s− 1) conditions (16 h light/8 h dark) or in continuous darkness. For the various wavelength experiments, after germination, Arabidopsis seedlings were grown under blue light (400–500 nm, 200 µmol m− 2s− 1) or red light (620–720 nm, 200 µmol m− 2s− 1). After germination, 10-day-old seedlings were inoculated with second-stage juveniles. Fifteen plants were used for each biological replicate.

Second-stage juvenile collection and inoculation

Meloidogyne incognita worms were maintained on a nematode-susceptible tobacco cultivar (Honghuadajinyuan) at the Nematode Institute of Northeastern China. Eggs were collected as described previously [20], with modifications. The roots were cut into pieces and then shaken with 10% commercial bleach for 5 min. The roots were poured through an 80-mesh sieve (180 μm), and the eggs were collected on a 500-mesh sieve (25 μm). The eggs were quickly purified by centrifugation in 35% sucrose for 10 min. The mixture was subjected to another round of centrifugation for 5 min and then rinsed three times in sterile water. The eggs were transferred to a modified Baermann pan at 25 °C in the dark, and the freshly hatched preparasitic second-stage RKN juveniles (J2s) were then harvested.

For RKN infection and development assays, ten days after the Arabidopsis seedlings geminated, three holes were dug around the Arabidopsis roots. One milliliter of 0.1% water‒agar mixture containing approximately 1000 J2s or water‒agar mixture alone was used as a treatment or control, respectively. At 18 days after inoculation, the seedlings were removed from the container for staining. The roots of the plants were treated with 10% bleach for 1 min, washed well with water, and boiled for 1 min in acid fuchsin solution (3.5% acid fuchsin in 25% acetic acid). After the solution cooled to room temperature, the acid fuchsin solution was washed away with water. The root material was then placed in 30 ml of glycerin acidified with a few drops of 6 N CH3COOH and heated to boiling [21]. Fifteen plants were used for each biological replicate. The number of galls and nematodes was counted using a Nikon SMZ800 stereomicroscope (Nikon, Japan). Nematode development was calculated by the following equation: juvenile nematode number/total number of nematodes. The standards for counting nematodes at different developmental stages are shown in Figure S2.

RNA extraction and quantitative PCR

Arabidopsis roots and leaves were harvested on Day 1 and Day 15 post-RKN inoculation (dpi) for gene expression investigation. Three independent biological replicates and three controls (plants at the same stage but without RKN inoculation) were used for RNA extraction at each time point. Total RNA was extracted using TRIzol reagent (Dingguo Biotechnology Co., Ltd., China). cDNA was synthesized from the extracted RNA samples using the PrimeScript RT reagent kit (Takara Bio, Japan) according to the manufacturer’s protocol.

Quantitative PCRs were performed in 96-well hard-shell PCR plates using a One Step SYBR PrimeScript RT‒PCR kit (Takara Bio, Tokyo, Japan) in a 20 µl volume. The reaction conditions were as follows: 95 °C for 30 s, 40 cycles at 95 °C for 5 s, and 60 °C for 30 s. Gene expression was calculated using the 2−ΔΔCt method. To ensure accurate qPCR results, the expression stability under nematode infection conditions of four candidate reference genes (AtACTIN1, AtACTIN8, AtOXA1 and AtUBP22) was evaluated using geNorm, NormFinder and BestKeeper analyses. The ATACTIN8 gene was used as an internal control for normalization of gene expression. Three technical replications were applied for each sample. All the primers used for quantitative PCR are shown in Table S1. T tests were utilized for measuring the significance of differences in gene expression, and p values were corrected with a false discovery rate (FDR).

Chromatin immunoprecipitation (ChIP) assays

Chromatin immunoprecipitation (ChIP) was performed as described previously [22], with slight modifications. Ten-day-old roots of HY5-GFP seedlings in the hy5 background were harvested. In brief, the samples were crosslinked using 1% formaldehyde for 15 min under a vacuum, and then 2 M glycine was added for an additional 15 min to terminate crosslinking. The samples were washed three times with ddH2O, frozen in liquid nitrogen and ground into a fine powder. We produced chromatin fragments (300∼500 bp) through sonication with a bioruptor (Bioruptor Plus; program 30 s on and 30 s off for 3 min). Anti-GFP-coupled Dynabeads were used for immunoprecipitation. After washing with low-salt wash buffer, high-salt wash buffer, LiCl wash buffer, and TE buffer, the samples were eluted with elution buffer. After the addition of 5 M NaCl, the samples were incubated overnight at 65 °C for reverse crosslinking. Immunoprecipitates were analyzed by semiquantitative PCR. Each input DNA level was used as an internal control. The PCR primers used for the ChIP assay are listed in Table S1.

Yeast one-hybrid analysis

The 386 bp AtSWEET11, 369 bp AtSWEET12, and 284 bp AtSWEET15 promoters were cloned and inserted into the pAbAi (Takara Bio, Japan) vector, and the open reading frame (ORF) sequence of AtHY5 was cloned and inserted into the pGAD7 (Takara Bio, Japan) vector. The appropriate pAbAi-AtSWEETs plasmid was transformed into the yeast strain Y1H Gold. Transformants containing each AtSWEETs promoter were used as competent cells and transformed with pGAD7-AtHY5 or a pGAD7 empty vector. The growth of yeast cells on -Leu synthetic dropout media was monitored.

Statistical analysis

All the data were analyzed using SPSS Statistics v.22.0. and GraphPad Prism 8 software. One-way analysis of variance (ANOVA) was conducted in this study. For ANOVAs, the data were tested for normality and equality of variations, and if necessary, natural log transformations were performed. All the data were analyzed using paired t tests and Tukey’s multiple comparison tests. The observed differences were found to be statistically significant (p < 0.05).

Results

Light is required for nematode infection and development

Throughout the plant’s life cycle, light, as an environmental signal, influences plant growth. To explore the influence of different wavelengths of light on nematode infection and development, we pretreated germinating Arabidopsis (Col-0) seedlings, which reached the soil surface under different wavelengths of light, to induce plant light responses to the different wavelengths, and inoculated them with RKN (Fig. 1a). The Arabidopsis seedlings demonstrated diverse development phases when exposed to the different wavelengths of light for 10 days (Fig. 1b). To explore the role of light in nematode infection and development, 10-day-old Arabidopsis seedlings were subjected to RKN penetration assays under different light conditions. The number of galls and nematodes significantly decreased in the dark. We therefore assessed these processes using red and blue light. There were more galls and nematodes under red light than under blue light, and the numbers of galls and nematodes under all light treatments were significantly greater than those under continuous darkness (Fig. 1c, d). Thus, RKN infection is affected by light signals.

Fig. 1
figure 1

(a) Schematic diagram of the nematode infection and development assays under different light conditions. (b) Growth phenotype of Arabidopsis thaliana under different light conditions at 10 dpi. Scale bar, 5 mm. (c) (d) Effects of light on M. incognita infection of Col-0 at 18 dpi, as determined by acid fuchsin solution staining. The data are the means ± SDs (n = 15). (*P < 0.05; **P < 0.01; ***P < 0.001, two-tailed t test)

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Response of the red light photoreceptor phytochrome to RKN parasitism in Arabidopsis

The Arabidopsis genome encodes five red light photoreceptor phytochromes (phyA–phyE) [23]. Among these genes, phyA and phyB are the most commonly reported to be associated with plant resistance [24, 25]. Col-0, phya-211, phyb-9, and phya/b seedlings were grown vertically on 1/2 MS medium under white light, and the observed root lengths of phya-211, phyb-9, and phya/b were significantly shorter than those of Col-0 (Figure S1). The number of galls was calculated at 18 days after inoculation, and significantly lower numbers of galls were observed on phya-211, phyb-9 and phya/b mutant roots than on wild-type roots (Fig. 2a). The total number of nematodes was lower in the roots of phya-211 and phya/b mutants than in those of the wild type. However, no significant difference was observed between the wild type and the phyb mutant (Fig. 2b). Compared with those in the wild-type control, juveniles were present in greater proportions in the phya-211 and phya/b mutants, but no differences were found in the phyb mutant (Fig. 2c). Compared with the nonnormalized phenotypic results, the numbers of galls and nematodes were generally higher in the phya-211 and phyb-9 mutants, possibly because the root weights of the phya-211 and phyb-9 mutants were much lower than that of Col-0 (Fig. 2d, e). At the same time, wild-type Arabidopsis seedlings were inoculated with J2 M. incognita, and qPCR analysis of the expression of the PHYA/PHYB gene was performed during the infection (1 dpi) and development (18 dpi) periods. In Arabidopsis leaves, PHYA exhibited the greatest increase (approximately 30-fold) at 18 dpi in response to RKN infection (Fig. 2f). In Arabidopsis roots, PHYA was induced at 1 dpi by RKN infection, and PHYA and PHYB were induced at 18 dpi (Fig. 2g).

Fig. 2
figure 2

(a) (b) (c) The fresh weight of each root was measured 18 days after inoculation of phya-211, phyb-9 or phya/b. The number of galls infected by nematodes and the ratio of juveniles to total nematodes in each root system per gram of root were analyzed. (d) (e) The number of galls and nematodes in each root system was analyzed. The data are the means ± SDs (n = 15). (f) (g) qPCR was used to quantify AtPHYA and AtPHYB expression at 1 dpi and 18 dpi in Arabidopsis. Three technical repeats were performed per sample. The Actin8 gene was used as an internal control. The error bars indicate the SDs of technical repeats (n = 3). (*P < 0.05; **P < 0.01; ***P < 0.001, two-tailed t test)

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Blue light photoreceptors cryptochrome and phototropin in the Arabidopsis response to RKN parasitism

Arabidopsis has two kinds of blue light photoreceptors, cryptochromes and phototropins [26]. cry1/2, phot1/2, and cry1/2 phot1/2 seedlings (mutants of the two types of blue light photoreceptors) were grown vertically on 1/2 MS medium under white light, and the lengths of the roots of cry1/2, phot1/2, and cry1/2 phot1/2 were significantly shorter than those of Col-0 (Figure S1). The cry1/2, phot1/2, and cry1/2 phot1/2 mutants and the wild type were used to analyze the effect of blue light signaling on RKN invasion and development. The number of galls was calculated at 18 days after J2 inoculation, and fewer galls were observed in the cry1/2, phot1/2, and cry1/2 phot1/2 mutants than in the wild type (Fig. 3a). Additionally, fewer total nematodes were detected in the cry1/2, phot1/2, and cry1/2 phot1/2 mutants than in the wild-type plants (Fig. 3b). Juveniles were present in greater proportions in cry1/2, phot1/2, and cry1/2 phot1/2 mutant roots (Fig. 3c). The normalized and nonnormalized phenotype results were the same for the blue light photoreceptor mutants (Fig. 3d, e). To further confirm the induction of CRY and PHOT by RKN, the expression of these genes was analyzed by qPCR during the infection (1 dpi) and development (18 dpi) periods. In Arabidopsis leaves, the expression of CRY1, PHOT1 and PHOT2 was significantly induced by RKN infection at 1 dpi compared with that in the control group. CRY1 and CRY2 were induced at 18 dpi compared with the control group (Fig. 3f). In Arabidopsis roots, CRY1, CRY2, PHOT1 and PHOT2 were induced at 18 dpi (Fig. 3g).

Fig. 3
figure 3

(a) (b) (c) The fresh weight of each root was measured 18 days after inoculation of cry1/2, phot1/2 and cry1/2 phot1/2. The number of galls infected by nematodes and the ratio of juveniles to total nematodes in each root system per gram of root were analyzed. The data are the means ± SDs (n = 15). (d) (e) The number of galls and nematodes in each root system was analyzed. (f)(g) qPCR was used to quantify AtCRY1, AtCRY2, AtPHOT1, and AtPHOT2 expression at 1 dpi and 18 dpi in Arabidopsis. Three technical repeats were performed per sample. The Actin8 gene was used as an internal control. The error bars indicate the SDs of technical repeats (n = 3). (*P < 0.05; **P < 0.01; ***P < 0.001, two-tailed t test)

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Photoreceptor-mediated RKN resistance through HY5

Photoreceptors sense and transduce light information to downstream signaling pathways. The transcription factor HY5 is located downstream of photoreceptors and plays an important role in the light signaling pathway. COP1 is a central negative regulator of photomorphogenesis that physically interacts with HY5 [27]. HY5 interacts with COP1 to specifically target HY5 for proteasome-mediated degradation in the nucleus [28]. hy5 and cop1-4 seedlings were grown vertically on 1/2 MS medium with a 12 h light photoperiod, and the root lengths of hy5 and cop1-4 were significantly shorter than that of Col-0 (Figure S1). The susceptibility of the hy5, pHY5:HY5-GFP hy5, and cop1-4 lines and the wild type to RKN infection was studied. The number of galls and nematodes in pHY5:HY5-GFP hy5 was not significantly different from that in the control group. However, in contrast to those in the wild type treatment, the number of galls and nematodes in hy5 was significantly lower, and the opposite phenotype was observed in cop1-4 (Fig. 4a, b). There was a greater proportion of juveniles in the roots of the hy5 mutant and a lower proportion of juveniles in the roots of the cop1-4 mutant than in the wild-type roots at 18 dpi. (Fig. 4c). The normalized and nonnormalized phenotype results were the same for the hy5 and cop1-4 mutants (Fig. 4d, e). The relative expression levels of the HY5 gene were determined during infection (1 dpi) and development (18 dpi). Compared with that in the control group, the expression of HY5 was significantly higher in the Arabidopsis leaves at 18 dpi (Fig. 4f). In the Arabidopsis roots, HY5 expression was suppressed at 1 dpi and induced at 18 dpi compared with that in the control group (Fig. 4f). However, COP1 expression was not induced after infection (Fig. 4g), indicating that HY5, rather than COP1, was the main nematode target gene. To further analyze whether HY5 is regulated by RKN infection, fluorescence microscopy was used to detect GFP signals in giant cells. The HY5-GFP signal indicated accumulation in giant cells (Fig. 4h).

Fig. 4
figure 4

(a) (b) (c) The fresh weight of each root was measured 18 days after inoculation of hy5, pHY5:HY5-GFP hy5 and cop1-4. The number of galls infected by nematodes and the ratio of juveniles to total nematodes in each root system per gram of root were analyzed. The data are the means ± SDs (n = 15). (d)(e) The number of galls and nematodes in each root system was analyzed. (f) (g) qPCR was used to quantify AtHY5 and AtCOP1 expression at 1 dpi and 18 dpi in Arabidopsis. Three technical repeats were performed per sample. The Actin8 gene was used as an internal control. The error bars indicate the SDs of technical repeats (n = 3). (*P < 0.05; **P < 0.01; ***P < 0.001, two-tailed t test). (h) Intensity of plants inoculated with the green fluorescent protein AtHY5-GFP and Meloidogyne incognita were measured by laser scanning confocal microscopy

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HY5 activates SWEETs by binding to its promoter directly

SWEETs provide bidirectional sugar transfer and are involved in the interaction of numerous pathogenic bacteria and plants. To date, 17 SWEET genes have been identified in Arabidopsis [29]. The expression of the clade III sucrose transporters AtSWEET11, 12 and 15 is significantly increased when plants are challenged with bacterial or fungal pathogens [29]. Infection of Arabidopsis by the protist Plasmodiophora brassicae led to the phloem-specific accumulation of the AtSWEET11 and AtSWEET12 proteins at the site of infection, which facilitated the delivery of sugars to the pathogen [30]. The atsweet11;12 double-knockout mutants were resistant to the hemibiotrophic fungus Colletotrichum higginsianum [31]. Infection with Botrytis cinerea enhances the expression of different AtSWEETs, principally AtSWEET15 [29]. AtSWEET11, 12 and 15 clearly exert their main functions during pathogen infection. HY5 is a transcription factor involved in light signaling pathways. It is possible that HY5 mediates the expression of the SWEET genes. To investigate this possibility, SWEET11, SWEET12 and SWEET15 expression was examined in the hy5 mutant. qPCR analysis revealed that the expression of the SWEET11, SWEET12, and SWEET15 genes was significantly lower in the hy5 mutant than in the wild type (Fig. 5a, b,c). As SWEET11, SWEET12 and SWEET15 are sensitive to HY5 expression, it is possible that HY5 acts as a transcriptional activator of SWEET11, SWEET12 and SWEET15. JASPAR analyses revealed that the HY5 transcription factor regulates downstream genes by binding to the G-BOX (CACGTG) and ACE-BOX (ACGT) motifs. Moreover, potential binding sites that can be regulated by HY5 were identified in the promoters of the SWEET11, SWEET12, and SWEET15 genes (Fig. 5d). To obtain evidence that HY5 binds directly to the SWEET11, SWEET12, and SWEET15 promoters, a ChIP assay was performed using promoter regions from the SWEET11, SWEET12, and SWEET15 loci and a HY5-GFP transgenic line. Root tissue from HY5-GFP lines was utilized for the ChIP assay. Fragments of approximately 40–140 bp from each part were amplified from immunoprecipitates isolated with anti-GFP antibodies. The SWEET11 promoter region was divided into five regions, and three regions located between bp 107 and 167, bp 1445 and 1470, and bp 1730 and 1787 from the translation start codon were amplified from the chromatin immunoprecipitates (Fig. 5e). The SWEET12 promoter region was divided into four regions, and two regions located between bp 577 and 620 and between bp 1454 and 1502 from the translation start codon were amplified from the chromatin immunoprecipitates (Fig. 5f). The SWEET15 promoter region was divided into four regions, and two regions located between bp 824 and 956 and between bp 1233 and 1289 from the translation start codon were amplified from the chromatin immunoprecipitates (Fig. 5g). ChIP indicated the presence of a HY5 cis-regulatory element in a fragment of the SWEET promoter. The results of this binding assay were confirmed using a yeast one-hybrid assay, which indicated that HY5 can activate the SWEET11, SWEET12 and SWEET15 promoters (Fig. 5h, i, j). Thus, the G-BOX and ACE-BOX are responsible for the binding of HY5. In summary, these data demonstrate that HY5 activates the transcription of SWEET11, SWEET12 and SWEET15 by binding the G-BOX and ACE-BOX cis-elements.

Fig. 5
figure 5

(a) (b) (c) qPCR was used to quantify AtSWEET11, AtSWEET12, and AtSWEET15 expression in Col-0 and hy5. Three technical repeats were performed per sample. The Actin8 gene was used as an internal control. The error bars indicate the SDs of technical repeats (n = 3). (*P < 0.05; **P < 0.01; ***P < 0.001, two-tailed t test). (d) Identification of HY5 binding motifs by the JASPAR program. The SWEET gene promoters were used for HY5 binding motif analysis. (e) (f) (g) Antiserum against green fluorescent protein (GFP) (Ab) and preimmune serum (Pre) were used for ChIP assays in Arabidopsis roots expressing HY5:GFP. The areas containing a G-BOX or ACE-BOX were amplified from immunoprecipitated DNA. Input DNA was used as an internal control. (h) (i) (j) A yeast one-hybrid assay was performed to analyze the HY5 activation of the 386 bp SWEET11, 369 bp SWEET12, and 284 bp SWEET15 promoters. Yeast cells harboring either pAbAi-p53 + pGAD7-53, pAbAi-AtSWEETs + pGAD7-AtHY5 or pAbAi-p53 + pGAD7 were grown on synthetic dropout media lacking Leu (-L)

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SWEETs negatively regulate RKN resistance

The responses of sweet11a, sweet12b, sweet15d, sweet11a/12b/15d and the wild type to RKN infection were investigated. Eighteen days after J2 inoculation, the number of galls was measured, and it was found that the sweet12b, sweet15d, and sweet11a/sweet12b/sweet15d mutant populations had many fewer galls than did the wild type (Fig. 6a). Additionally, the total number of nematodes was lower in the roots of sweet12b, sweet15d, and sweet11a/12b/15d than in those of the wild-type control (Fig. 6b). Juveniles were present in greater proportions in sweet11a, sweet12b, sweet15d and sweet11a/12b/15d mutants (Fig. 6c). To investigate whether AtSWEET11, AtSWEET12 and AtSWEET15 specifically accumulated in galls after infection, GUS expression patterns upon RKN infection in Arabidopsis plants expressing AtSWEET11-GUS, AtSWEET12-GUS and AtSWEET15-GUS under the control of the endogenous promoter were analyzed. Strong AtSWEET11-GUS and AtSWEET12-GUS signals were observed within the developing knot of M. incognita in Arabidopsis roots. However, AtSWEET15-GUS was not detected, perhaps because AtSWEET15 was not expressed in Arabidopsis roots (Fig. 6d). The normalized and nonnormalized phenotype results were the same in the sweet mutants (Fig. 6e, f). qPCR analysis revealed that the expression of the AtSWEET11 and AtSWEET12 genes in Arabidopsis roots was significantly induced by RKN infection at 18 dpi compared with that in the control group (Fig. 6g, h).

Fig. 6
figure 6

(a) (b) (c) The fresh weight of each root was measured 18 days after inoculation of the sweet11a, sweet12b, sweet15d and sweet11a/12b/15d mutants. The number of galls infected by nematodes and the ratio of juveniles to total nematodes in the roots were analyzed. The data are the means ± SDs. (d) Histochemical GUS assay of AtSWEET11-GUS, AtSWEET12-GUS and AtSWEET15-GUS lines infected with J2s of M. incognita. Strong GUS activity at the nematode feeding sites was observed. (e)(f) The number of galls and nematodes in each root system was analyzed. (g) (h) qPCR was used to quantify AtSWEET11 and AtSWEET12 expression at 1 dpi and 18 dpi in Arabidopsis thaliana. Three technical repeats were performed per sample. The Actin8 gene was used as an internal control. The error bars indicate the SDs of technical repeats (n = 3). (*P < 0.05; **P < 0.01; ***P < 0.001, two-tailed t test)

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Discussion

Despite extensive research on the interaction between nematodes and plants [32,33,34,35,36,37], limited knowledge exists regarding the regulatory mechanisms employed by nematodes to facilitate nutrient transport from hosts for their own sustenance. Our studies showed that the light signaling pathways and sugar transporters of Arabidopsis are regulated by RKN infection and feeding.

Light signaling plays a crucial role in regulating physiological processes during normal growth and development, as well as in plant defense responses. Red light has been found to induce systemic resistance against Meloidogyne incognita in watermelon and tomato [38, 39]. Pretreatment of Arabidopsis with red light (600–700 nm) induces systemic resistance against M. incognita [40]. In this study, we found that the number of galls and nematodes in the continuous darkness treatment group was significantly lower than that in the light treatment groups. To investigate the effects of different wavelengths of light on RKN infection and development, we treated RKN-infected Arabidopsis seedlings with red and blue light. The results showed that the number of galls and nematodes under red and blue light conditions was significantly greater than that under continuous darkness. Therefore, different wavelengths of light affect the infection and development of nematodes in Arabidopsis. In our experiments on the effects of different light regimes on nematode infection, we found that different light regimes lead to morphological and physiological differences, especially because dark treatment leads to shorter roots, and the absolute nematode number does not reflect whether nematode susceptibility is caused by the immune response or root morphology. To reduce the effect of this morphological difference, we used the number of nematodes normalized to the root mass to analyze susceptibility. Nontargeted plant response analyses, such as transcriptome or metabolome analyses, may be useful. The differences in root morphology and nematode susceptibility warrant further investigation.

Dedicated photoreceptors help plants perceive light signals of different wavelengths [41]. Phytochromes (Phys) detect red/far-red light in the range of 600–750 nm; phytochromes exist in two interconvertible forms, Pr and Pfr, which absorb red and far‐red light, respectively. They are synthesized in an inactive Pr form in the cytosol and translocated to the nucleus after conversion to the Pfr form by the absorption of red light. Photoactivated phytochromes move into the nucleus and modulate the activity of several transcription factors [42]. To evaluate the effect of nematode infection on these photoreceptors, we inoculated phytochrome mutants with nematodes. The number of galls and nematodes in phya-211 and phya/b was significantly lower, and the proportion of juveniles to total nematodes was higher. Moreover, the expression of the PHY gene was significantly induced by RKN infection compared with that in the control group. Cryptochromes (CRYs) and phototropins (PHOTs) detect blue light in the range of 315–400 nm. After perceiving different wavelengths of light, these photoreceptors further transmit signals through a cascade to modulate the expression of multiple genes [42]. In addition, after we inoculated cryptochrome and phototropin mutants with J2 RKNs, the number of galls and nematodes in cry1/2, phot1/2 and cry1/2phot1/2 was significantly lower, and the proportion of juveniles to total nematodes was higher. The expression levels of the CRY and PHOT genes were significantly greater in the RKN-infected group than in the control group. Taken together, our results indicate the importance of photoreceptors in host–nematode interactions.

The bZIP transcription factor HY5 plays critical roles in light signaling. HY5 acts as a positive regulator of light signaling. HY5 was shown to bind to the G-box motif in experiments with fragments of the chalcone synthase gene promoter [43]. When we inoculated the hy5 and pHY5:HY5-GFP hy5 mutants with nematodes, we found that the number of galls and nematodes in hy5 was significantly lower, and the proportion of juveniles to total nematodes was higher; there was no difference in the pHY5:HY5-GFP hy5 mutant. qPCR analysis of the expression of the HY5 gene in Col-0 showed that HY5 was significantly induced in the roots by RKN infection relative to the control group. Fluorescence microscopy was used to detect a GFP signal in giant cells; HY5-GFP was found to be accumulated in giant cells. HY5 activity is regulated by the CONSTITUTIVELY PHOTOMORPHOGENIC 1 (COP1) and SUPPRESSOR OF PHYA 1 (SPA1) complex, which destabilizes HY5 via the E3 ligase activity of COP1 in the nucleus, which causes the ubiquitylation necessary for 26 S proteome-mediated degradation [44, 45]. The present study revealed that the number of galls and nematodes in cop1-4 increased significantly, and the proportion of juveniles to total nematodes decreased. The COP1 gene was induced by RKN infection.

During pathogen infection, pathogens are capable of inducing metabolic and transcriptomic modifications in their hosts. Sugar metabolism and mobilization are greatly affected during infection. The induction of plant SWEET transporters by pathogens has been linked to an increased capacity of pathogens to obtain host-derived sugars for nutrition [46]. AtSWEET11 and AtSWEET12 localize to the plasma membrane of the phloem, and AtSWEET11 and AtSWEET12 mutations restrict intercellular sucrose transport to the interface of adjacent phloem cells to prevent pathogen infections [47]. Plants promote root growth under drought stress by regulating AtSWEET11 and AtSWEET12, enhancing exoplasmic phloem loading at source tissues and unloading at root sink tissues to transport sucrose from shoots to roots [48]. Our results revealed that the number of galls and nematodes were significantly lower in sweet12b, sweet15d, and sweet11a/sweet12b/sweet15d, and the proportion of juveniles to total nematodes was greater. Nematode infection induces AtSWEET11 and AtSWEET12 in root tissues. The expression of AtSWEET15 and AtSWEET15-GUS was not detected in roots due to the accumulation of SWEET15 in the epidermal cells of the seed coat; SWEET15 is unlikely to contribute to the phloem export of sucrose [49]. The mechanism by which SWEET15 negatively regulates the infection and development of nematodes needs further investigation. Genome-wide ChIP-chip experiments demonstrated that HY5 regulates the expression of nearly one-third of genes in Arabidopsis, and ~ 3000 of these genes are directly controlled by HY5 binding [50]. HY5 activates the transcription of SWEET11, SWEET12 and SWEET15 by binding the G-BOX and ACE-BOX cis-elements, thus affecting nematode infection and development in Arabidopsis.

In our experiments in which different mutants were infected with nematodes, we found that phya-211 and phyb-9 exhibited meaningful differences between normalized and nonnormalized nematode or gall counts, possibly because the root weights of the phya-211 and phyb-9 mutants are much lower than that of Col-0, resulting in a general increase in the normalized mutant phenotype results. The root weight and nematode susceptibility of the mutants warrant further investigation.

Conclusions

Light is an important living factor for plants and pathogenic organisms. In this study, we showed that the expression of the enzyme ELONGATED HYPOCOTYL5 (HY5) is significantly induced by infection with Meloidogyne incognita. HY5 inhibits hypocotyl growth and lateral root development and has transcriptional activation activity in Arabidopsis. Genetic analysis of a HY5 genome-edited mutant and revertant plants demonstrated that HY5 negatively regulates plant resistance to RKN. Expression level and genetic analyses revealed that the photoreceptor genes PHY, CRY, and PHOT have a negative impact on nematode infection. qPCR analysis revealed that HY5 activates SWEET11a, SWEET12b and SWEET15d, three SWEET family sugar transporter genes. The sweet11a, sweet12b, sweet15d and sweet11a/sweet12b/sweet15d mutants are less susceptible to RKN than are wild-type plants, suggesting that these three SWEETs negatively regulate plant resistance. ChIP and yeast one-hybrid assays revealed that HY5 directly activates SWEET11a, SWEET12b and SWEET15d by binding to their promoter fragments. These results indicate that HY5 activates SWEET11a, SWEET12b and SWEET15d to negatively regulate plant resistance. Our work on the relationship between HY5 and sugar transporters should provide useful information for scientists seeking to understand the effects of light signaling regulation on root-knot nematode infection and development.

Data availability

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

Abbreviations

HY5:

ELONGATED HYPOCOTYL 5

COP1:

CONSTITUTIVELY PHOTOMORPHOGENIC 1

PHYA, B:

Phytochrome A, B

CRY1,2:

Cryptochrome 1, 2

PHOT1,2:

Phototropin 1, 2

RKN:

Root-knot nematode

bZIP:

Basic-region leucine zipper

ChIP:

Chromatin immunoprecipitation

Y1H:

Yeast one-hybrid

dpi:

Days postinoculation

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Funding

This research was funded by the National Key R&D Program of China (2023YFD1400400), the National Natural Science Foundation of China (32272499), and the National Parasitic Resources Center (abbreviation number: NPRC-2019-194-30) and supported by the China Agriculture Research System of MOF and MARA (CARS-04-PS13).

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Authors and Affiliations

  1. Nematology Institute of Northern China, College of Plant Protection, Shenyang Agriculture University, Shenyang, China

    Bohong Wu, Xueying Jia, Wei Zhu, Yin Gao, Yuxi Duan, Lijie Chen, Haiyan Fan, Yuanhu Xuan & Xiaofeng Zhu

  2. College of Biological Science and Technology, Shenyang Agriculture University, Shenyang, China

    Yuanyuan Wang

  3. College of Sciences, Shenyang Agriculture University, Shenyang, China

    Xiaoyu Liu

  4. Helongjiang Academy of Agricultural Sciences, Qiqihar, China

    Kefei Tan

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Contributions

WBH, JXY, ZW, GY and TKF conceived and wrote the manuscript. DYX, CLJ, FHY, WYY, LXY, XYH and ZXF revised the manuscript. All authors have read and agreed to the published version of the manuscript.

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Wu, B., Jia, X., Zhu, W. et al. Light signaling regulates root-knot nematode infection and development via HY5-SWEET signaling. BMC Plant Biol 24, 664 (2024). https://doi.org/10.1186/s12870-024-05356-2

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