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Resistance mechanism of Abies beshanzuensis under heat stress was elucidated through the integration of physiological and transcriptomic analyses

BMC Plant Biology volume 25, Article number: 621 (2025) Cite this article

Abstract

Elevated temperatures significantly impaired the normal growth and development of plants. This study combined physiological and transcriptomic analyses to explore the potential mechanisms of response to heat stress in Abies beshanzuensis M. H. Wu. Under heat stress, A. beshanzuensis exhibited reduced photosynthetic rates and chlorophyll content, accompanied by marked downregulation of photosynthesis-associated genes, suggesting heat-induced photoinhibition and compromised carbon assimilation capacity. Furthermore, the increased activities of MDA, SOD, POD, and CAT suggested that A. beshanzuensis could withstand heat stress by enhancing the activity of antioxidant enzymes to mitigate excess reactive oxygen species and anions. Transcriptome analysis revealed the induction of genes related to heat shock proteins, plant hormone signaling, and antioxidants, which could enhance the tolerance of A. beshanzuensis to high temperatures. In summary, the research demonstrated that A. beshanzuensis could not tolerate high temperatures, which was identified as one of the primary reasons for its endangerment. This study offers a novel approach to investigating the regulatory mechanisms of heat stress.

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Introduction

The increasing global climate change is driving a notable rise in both the intensity and frequency of extreme high temperatures in recent decades [1]. Seasonal warming across various global regions may result in peak temperatures that exceed annual averages [2]. Heat stress adversely affects plant physiology, compromising growth, reproduction, and yield [3]. Photosynthesis, a crucial process in plant physiology, is particularly sensitive to elevated temperatures [4]. Elevated temperatures can reduce photosynthetic efficiency by impairing light energy absorption through chlorophyll degradation, disrupting chloroplast ultrastructure, and inactivating ribulose bisphosphate carboxylase/oxygenase [5]. Consequently, excessive light energy under high temperatures can induce photoinhibition [6]. Photosystem II (PSII), which plays a pivotal role in the photosynthetic light reactions, is particularly vulnerable to thermal stress within the photosynthetic apparatus [7]. Chlorophyll fluorescence is a valuable indicator of light absorption, transmission, distribution, and energy dissipation within PSII, and is widely used to assess plant photosynthetic performance [8, 9]. Under extreme heat stress conditions, key photosynthetic parameters, such as the electron transport rate (ETR), photosynthetic efficiency (Yield), non-photochemical quenching (NPQ), and photochemical quenching (QP), show significant reductions, which may be attributable to PSII damage [10, 11].

Heat stress leads to physiological damage in plants. In response, plants activate complex physiological pathways to mitigate such damage. Osmotic regulation is a critical mechanism for plant resilience under heat stress [12]. Under stressful conditions, plants increase the levels of osmotic regulatory substances to maintain optimal water balance in leaves and minimize cellular or tissue damage [13]. Concurrently, elevated temperatures promote the generation of reactive oxygen species (ROS) and lipid-peroxidation products such as malondialdehyde (MDA), exacerbating oxidative injury [14]. To detoxify these harmful compounds, plants upregulate antioxidant enzymes, notably superoxide dismutase (SOD), catalase (CAT) and peroxidase (POD), which together dismantle ROS and repair membrane integrity [15]. Thus, coordinated osmolyte accumulation and dynamic modulation of antioxidant defenses underpin plant resilience to heat‐induced oxidative stress.

At the transcriptional level, heat stress activates a regulatory network that induces the marked upregulation of heat shock proteins (HSPs). These molecular chaperones play dual protective roles by safeguarding cellular homeostasis and mediating stress signaling transduction under thermal stress [16, 17]. In poplar (Populus × euramericana), for instance, PeHSFA3 was strongly upregulated under heat treatment, playing a protective role in cellular stability [18]. In Paeonia suffruticosa, PsHSP17.8, PsHSP21 and PsHSP27.4 enhanced heat resistance by increasing SOD activity and proline content [17]. Beyond classical HSFs, other TF families such as NAM-ATAF1/2-CUC2 (NAC), Myeloblastosis (MYB) and basic leucine zipper (bZIP) and have also been implicated in heat stress responses [19,20,21]. In addition to direct transcriptional regulation, phytohormone signaling plays a pivotal role in modulating heat stress responses [22]. Together, these findings highlight the multifaceted nature of transcriptional and hormonal regulation under heat stress.

Abies beshanzuensis M. H. Wu, an ancient relict plant from the fourth Glacial period, is often referred to as a “living fossil” or the “plant giant panda.” However, only three wild adult plants remain, placing the species in a critically endangered state that necessitates urgent conservation efforts. With the escalation of global warming, future temperature increases are predicted to lead to more frequent short-term extreme heat events. Previous studies have shown that global warming has led to the widespread loss of suitable habitats for A. beshanzuensis, exacerbating its endangerment [23]. The extent of suitable habitats for A. beshanzuensis closely correlates with its tolerance to elevated temperatures. Therefore, understanding the physiological and molecular mechanisms of A. beshanzuensis in response to heat stress, as well as its tolerance thresholds, is of paramount importance. This research not only provides insight into the underlying causes of its endangerment but also has crucial implications for developing in-situ and ex-situ conservation strategies in response to climate change. In conclusion, this study aims to explore the mechanisms behind the endangerment of A. beshanzuensis by investigating its physiological and molecular responses to varying altitudes and heat stress gradients, thereby providing a scientific basis for its protection.

Materials and methods

Plant materials, growth conditions, and different light intensities

In this study, the grafted seedlings of Abies beshanzuensis M. H. Wu produced in 2018 were selected as the experimental materials. Seedlings that showed consistent growth and health conditions were carefully selected and placed in an artificial climate cultivation box for a 20-day period of adaptability training. The A. beshanzuensis were divided into four treatment groups: 25 °C/20°C (Room temperature group, Control); 30 °C/25°C (Mild high-temperature group, MS); 35 °C/30°C (Middle high-temperature group, MTS); and 40 °C/35°C (High-temperature group, HTS). Each treatment received a light intensity of 400 µmol m− 2 s− 1, with a 12-hour light/12-hour dark (LD 12:12), and the relative humidity was maintained at about 85%. Uniform watering was conducted every evening to prevent drought stress induced by high temperatures. Sampling was carried out before treatment (0 days) and on the 3rd, 6th, 9th, and 12th days after treatment for each group. During each sampling event, leaves from corresponding sections of branches from the current year were collected, combined, quickly frozen using liquid nitrogen, and subsequently stored at -80 °C for the analysis of physiological indicators, transcriptome sequencing and qRT-PCR. All index figures were measured three times.

Determination of chlorophyll fluorescence parameters

The chlorophyll fluorescence parameters of seedlings under various temperature treatments were measured using a Mini-PAM (Walz, Effeltrich, Germany) and WinControl 3 software (Walz, Effeltrich, Germany). Initially, the leaves were dark-adapted for 0.5 h. Subsequently, the instrument’s internal light source was used to measure Yield, ETR, qP, and NPQ under different light intensities. The experiment was repeated three times for validation.

Determination of chlorophyll content

Leaves from A. beshanzuensis, which had undergone various temperature treatments, were finely cut and homogenized. Approximately 0.2 g of each sample was weighed in a mortar, combined with a small amount of quartz sand and 80% acetone, and ground to create a homogenate. This mixture was then extracted for 2 h until the tissue turned white, followed by filtration. The resulting filtrate was collected in a 25 mL volumetric flask and adjusted to volume using an 80% acetone solution. A blank control was prepared using the same solvent. According to the Lambert-Beer law, the relationship between chlorophyll a (Chl a) and chlorophyll b (Chl b) content, and absorbance values at various wavelengths, was expressed as follows [24]:

Chl a= (12.71A663- 2.59A645) ×V/ (1000×FW).

Chl b= (22.88A645- 4.76A663) ×V/ (1000×FW).

Where A663 and A645 represent the absorbance values at their respective wavelengths, V is the volume of the extraction solution (mL), and FW is the fresh weight of the leaf.

Determination of soluble sugar, soluble protein, and proline content

The proline content (µg/mL) was determined using the method described by Bates et al. [25]. 0.1 g of leaf sample was homogenized with 1 mL of extraction solution, centrifuged at 8,000×g for 10 min, and the supernatant was collected. Absorbance was measured at a wavelength of 520 nm.

The soluble sugar content (µg/mL) was determined using the phenol-sulfuric acid method described by Dubois et al. [26]. 0.5 g of A. beshanzuensis leaves were weighed, added with water, and homogenized at a 1:25 ratio. The mixture was then extracted via ultrasonic soaking for 1 h. Subsequently, 1 milliliter of the leaf extract was combined with 5 milliliters of anthracene sulfate reagent (containing 1 gram of anthracene per 1 L of 80% sulfuric acid solution). The mixture was boiled in a water bath for 10 min and cooled to room temperature. The absorbance at 620 nm was measured using an ultraviolet spectrophotometer.

Soluble protein content was determined using the Coomassie brilliant blue G-250 method [27]. 0.5 g of sample blades were homogenized by grinding with water at a 1:25 ratio. The homogenized mixture was subsequently centrifuged at 4 °C at 10,000×g for 10 min and stored for later analysis. A. beshanzuensis leaf extract (0.1 mL) was mixed with 4.9 mL of Coomassie Bright Blue G-250 solution, and the absorbance at 595 nm was then measured.

Determination of enzyme activity

The malondialdehyde (MDA) content in the leaves was measured using the thiobarbituric acid method [28]. 0.1 g leaf sample was homogenized in 1 mL of extraction solution on ice, centrifuged at 8,000×g at 4 °C for 10 min, and the supernatant was collected. Absorbance at 532 nm and 600 nm was measured with a blank control, and ΔA532 and ΔA600 were calculated as the differences between sample and blank absorbance values. MDA content was calculated using the formula:

MDA content (nmol/g) = 32.258×(ΔA532 − ΔA600)/W.

W: weight (g).

The activities of superoxide dismutase (SOD), catalase (CAT), and peroxidase (POD) were determined using commercial kits from Beijing Solabao Technology Co., Ltd. (Beijing, China), following the manufacturer’s instructions.

For SOD activity, leaf samples (0.1 g) were homogenized in 1 mL of extraction solution on ice, centrifuged at 8,000×g at 4 °C for 10 min, and the supernatant was collected. Absorbance values for Adetermination, Acontrol, A1 blank and A2 blank at 560 nm were recorded. ΔA determination and ΔA blank were calculated as Adetermination − Acontrol and A1 blank − A2 blank, respectively. SOD activity was calculated using the following formulas:

Inhibition percentage= (ΔAblank − ΔAdetermination)/ΔAblank×100%.

SOD activity (U/g mass) = 11.4×Inhibition percentage/ (1 − Inhibition percentage) ×W×F.

W: weight (g); F: dilution ratio.

For CAT activity, the preparation of samples followed the same protocol as for SOD. Absorbance values at 405 nm for Aassay, Acontrol, Ablank and Astandard were recorded. ΔAassay, and ΔAstandard were calculated as Aassay − Acontrol and Astandard−Ablank, respectively. CAT activity was calculated as:

CAT activity (U/g mass) = 10 × (ΔAstandard − ΔAassay / ΔAstandard) / W × F.

F: Sample dilution ratio; W: Sample weight (g).

For POD activity, the preparation of samples followed the same protocol as for SOD. Absorbance values at 470 nm were recorded as A1 (at 30 s) and A2 (at 1 min), and ΔA was determined as A2 − A1. POD activity was calculated using the formula:

POD activity (U/g mass) = ΔA × Vt / (W × Vm / Vs) / 0.01 / T = 7133 × ΔA / W.

Vt: Total reaction volume (1.07 mL); Vm: Sample volume added (0.015 mL); Vs: Extraction solution volume (1 mL); T: Reaction time (1 min); W: Sample weight (g).

RNA sequencing and RT–qPCR analysis

Total RNA extraction was performed using the Trizol Invitgen kit (CA, USA), followed by assessment of RNA quality and purity using the 2100 Bioanalyzer and RNA 1000 Nano LabChip Kit (Agilent, CA, USA). Subsequently, paired-end sequencing was conducted on the Illumina Novaseq™6000 platform (LC Sciences, USA), with both RNA extraction and sequencing handled by Lianchuan Biotech Company.

The sequencing data underwent de novo assembly. Initially, CutAdapt and Perl scripts were utilized to remove read fragments containing adapter contamination, low-quality bases, and undetermined bases. Following this, sequence quality was validated using FASTQC. Trinity 2.4.0 was employed for de novo assembly of the transcriptome. Trinity organized transcripts into clusters based on shared sequence content, referred to as “genes,” with the longest transcript in each cluster chosen as the representative “gene” sequence (Unigene).

Unigene expression levels were quantified using Salmon analysis software to calculate TPM. The R Package Edger was used to filter statistically significant (P1) results. Metabolic pathway analysis was conducted using GO (http://www.geneontology.org) and KEGG (http://www.genome.jp/kegg/). The raw data from the sequenced transcriptome have been deposited in the Gene Expression Omnibus at National Center for Biotechnology Information Database (NCBI) under accession number PRJNA1064174.

For the qRT-PCR analysis, cDNA synthesis utilized the HiScript® III All-in-one RT SuperMix kit (Vazyme, Nanjing, China), followed by RT-qPCR conducted on the QuantStudio3 platform. Six differentially expressed genes, common across all four treatment groups, were selected randomly. Primers were designed with Primer Premier 6.0, and their sequences are detailed in Table S1. Primer synthesis was outsourced to Shanghai Shenggong Bioengineering Company. The Actin gene of Masson pine served as the internal reference [29]. Relative expression levels of the six differentially expressed genes were assessed using the 2−∆∆CT method. Each qRT-PCR experiment included three biological replicates and three technical replicates.

Statistical analysis

Analysis of variance was performed using SPSS v21.0 software. Data visualization was performed using GraphPad Prism 9.0. For the data of the experiments, one-way ANOVA with Duncan’s discount was used to determine significant differences, with a P < 0.05 considered statistically significant.

Results

Effects of heat stress on the morphological in A. beshanzuensis

To investigate the morphological and physiological responses of A. beshanzuensis to heat stress, seedlings were exposed to four distinct environments (Control, MS, MTS, and HTS) over a period of 20 days. Significant variations in the growth inhibition of A. beshanzuensis were observed under heat stress conditions (Fig. 1). In the MTS treatment group, there were no notable changes in the morphology of A. beshanzuensis leaves during the initial 6 days. However, by the 9th and 12th days, certain leaf bases showed yellow-brown spots, which eventually turned yellow-brown in color. Additionally, by the 3rd day at the HTS level, the majority of leaves exhibited yellow-brown spots. With increasing exposure duration, nearly all leaves had turned yellow-brown by the 12th day.

Fig. 1
figure 1

Changes of leaf phenotype of A. beshanzuensis seedlings with stress time under different degrees of high temperature stress. (A) Control; (B) MS; (C) MTS; (D) HTS

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High temperature stress attenuated the photosynthetic capacity of A. beshanzuensis

A. beshanzuensis exhibited a rapid decline in Yild and ETR under heat stress conditions (Fig. 2A and B). Furthermore, these parameters showed a positive correlation with exposure duration, with the lowest values observed after 12 days of stress, indicating significant inhibition in both photosynthetic efficiency and relative electron transfer. In the HTS treatment group, the qP value declined rapidly after 3 days of stress, indicating damage to the PSII reaction center due to high temperature, leading to reduced activity of the photosynthetic reaction center (Fig. 2C). NPQ, which represents the excitation energy absorbed by photosystem II and dissipates heat energy through regulation of the photoprotective mechanism, experienced a rapid and significant decrease in A. beshanzuensis on the 6th day under HTS stress, highlighting severe damage to the photoprotective mechanism (Fig. 2D).

Fig. 2
figure 2

Changes of photosynthetic capacity and chlorophyll content of A. beshanzuensis under heat stress. (A) photosynthetic efficiency; (B) Electron transport rate (ETR); (C) and photochemical quenching (QP); (D) Non-photochemical quenching (NPQ); (E) Chlorophyll a (Chl a) content; (F) Chlorophyll b (Chl b) content. Data are mean ± SD (n = 3). Different uppercase letters at the top of the bar indicate significant differences between different stress times (P < 0.05). Different lowercase letters indicate a significant difference between different temperature stresses (P < 0.05)

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Changes of chlorophyll content of A. beshanzuensis under heat stress

High temperature stress significantly reduced the levels of chlorophyll a and b in A. beshanzuensis (Fig. 2E and F). Peak concentrations of chlorophyll a and chlorophyll b were observed in the Control and MS treatment groups. In contrast, chlorophyll a and chlorophyll b content in leaves of A. beshanzuensis decreased progressively with prolonged stress duration in the MTS and HTS treatment groups, reaching their lowest levels at 12 days of stress. Compared to the Control, there was a 64.58% reduction in chlorophyll a content and a 61.20% reduction in chlorophyll b content.

Changes of antioxidant capacity of A. beshanzuensis under heat stress

In the MTS treatment group, both MDA content and SOD activity gradually increased, reaching their peak at 12 days of stress exposure. Interestingly, an initial surge in MDA content in this group was followed by a subsequent decline, which may correlate with the observed heat stress resilience in A. beshanzuensis (Fig. 3A and B). Under MTS stress, POD activity showed a steady rise, while in the MTS group, an initial increase in POD activity was followed by a decrease, peaking at 6 days of stress exposure (Fig. 3C). In both MTS and HTS stress conditions, CAT activity initially decreased and then increased, reaching peak levels at 12 days and 6 days, respectively (Fig. 3D). Overall, under MTS and HTS stress, the activities of MDA, SOD, POD, and CAT in A. beshanzuensis exceeded those observed in untreated counterparts. These findings suggest that A. beshanzuensis enhances antioxidant enzyme activity to mitigate the accumulation of reactive oxygen species and anions under heat stress conditions. Soluble sugars, soluble proteins, and free proline are known to enhance plant resilience to heat stress. Importantly, our results indicated a significant increase in the levels of these components under both MTS and HTS stress conditions (Fig. 3E-G).

Fig. 3
figure 3

Antioxidant capacity of A. beshanzuensis under heat stress. (a) Quantitative analysis of MDA content. (B) Superoxide dismutase (SOD) activity; (C) Catalase (CAT) activity; (D) Peroxidase (POD) activity; (E) Total proline contents; (F) Soluble sugars contents; (G) Total soluble proteins contents. Data are mean ± SD (n = 3). Different uppercase letters at the top of the bar indicate significant differences between different stress times (P < 0.05). Different lowercase letters indicate a significant difference between different temperature stresses (P < 0.05)

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Key metabolic pathways in response to high temperature stress were identified through KEGG enrichment analysis and GO analysis of DEGs

Differentially expressed genes were identified across various treatment groups. Specifically, the analysis revealed 1868, 3580, and 9344 DEGs in the Control vs. MS, Control vs. MTS, and Control vs. HTS comparisons, respectively (Fig. S1). A volcano plot illustrating these DEGs in the leaves of A. beshanzuensis subjected to different levels of heat stress depicted the fold change in gene expression and the significance of these differences (Fig. S1A-C). These results clearly indicate significant changes in gene expression levels in A. beshanzuensis under heat stress.

To further explore the primary biological functions performed by DEGs under varying temperature treatments, we conducted GO enrichment analysis on DEGs from different high-temperature treatment groups and the control group (Fig. 4A). Under heat stress, A. beshanzuensis significantly activates biological pathways associated with response to heat, flavonoid biosynthetic process and DNA binding transcription factor activity, suggesting a coordinated strategy to maintain cellular homeostasis through antioxidant metabolism and transcriptional reprogramming.

Fig. 4
figure 4

GO and KEGG pathway enrichment analyses of DEGs in leaves of A. beshanzuensis under heat stress. (A) GO pathway enrichment analyses of DEGs; (B) KEGG pathway enrichment analyses of DEGs in (B) MS vs. Control, (C) MTS vs. Control and (D) HTS vs. Control. The y‑axis lists the pathway names, and the x‑axis shows the enrichment factor — the ratio of enriched gene/transcript counts in the sample to the annotated gene/transcript counts in the background. A higher enrichment factor indicates a stronger enrichment. The size of each point reflects the number of genes in that pathway, and the color of each point corresponds to a specific Q‑value range. Only the top 30 enriched pathways with p < 0.05 are displayed

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Furthermore, KEGG metabolic pathway analysis was performed on DEGs from various high-temperature treatments and the control group, revealing the top 30 significantly enriched KEGG pathways (P < 0.05) (Fig. 4B-D). In MH, differentially expressed genes are significantly enriched in flavonoid biosynthesis, phenylpropanoid biosynthesis, oxidative phosphorylation and glycolysis. Moreover, significant enrichment of heat shock–related pathways underscores their pivotal roles in mitigating oxidative damage (Fig. 4B). In MTS, A. beshanzuensis orchestrates its adaptive response by flavonoid biosynthesis, phenylpropanoid biosynthesis, glycolysis and MAPK signaling pathways (Fig. 4C). Furthermore, the HTS exhibited significant enrichment in genes associated with flavonoid biosynthesis, phenylpropanoid biosynthesis, plant hormone signal transduction and photosynthesis - antenna proteins (Fig. 4D).

To validate the reliability of the RNA-seq data, qRT-PCR analysis was conducted on six DEGs. The expression patterns of these six DEGs across different temperature treatment groups were consistent with the transcriptome sequencing results, confirming the high reliability of the RNA-seq data (Fig. S2).

Changes of DEGs in A. beshanzuensis under heat stress

Heat stress reduced the photosynthetic rate of A. beshanzuensis, prompting us to investigate the expression patterns of photosynthesis-related DEGs (Fig. 5 and Table S2). Genes associated with photosynthesis showed significant down-regulation in both MHS and MTS compared to Control, including 6 Pet, 10 Psa, 10 Psb, 1 Ycf, and 1 PPL gene. These results confirm that high temperature stress markedly suppresses the expression of photosynthesis-related genes, leading to a decrease in the photosynthetic rate.

Fig. 5
figure 5

Heat maps showed the expression patterns of photosynthesis-related genes in A. beshanzuensis under heat stress. The data in the figure are FPKM of DEGs. The color gradient in the heatmap, transitioning from blue to red, signifies a gradual increase in gene expression levels

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To assess the antioxidant capacity of A. beshanzuensis, we analyzed the expression patterns of DEGs associated with antioxidants (Fig. 6 and Table S3). After exposure to heat stress, the expression levels of four heat shock proteins decreased significantly. Our analysis indicated notable down-regulation of genes involved in REDOX processes, such as glutathione S-transferase (GST and PRP1), glutamyl cyclitransferase (GGCT), Microsomal Glutathione S-Transferase 3 (Mgst3), NADH-ubiquinone oxidoreductase chain 1 (ND1), cytochrome c oxidase subunit 2 (COX2), NADH dehydrogenase (MEE4), and Cytochrome b (MT-CYB). Interestingly, genes associated with ATP synthase were up-regulated, possibly indicating A. beshanzuensis need for energy to maintain ecological balance following heat stress. The upregulation of the Superoxide dismutase (SOD) gene suggests removal of excess ROS and maintenance of optimal cellular ROS levels. Within the MTS, genes linked to the ABC transporter showed significant upregulation. Compared with the control, key structural genes governing flavonoid biosynthesis exhibited marked transcriptional suppression in the treatment group, including ANR (anthocyanidin reductase), CHI3 (chalcone isomerase 3), AN3 (anthocyanin 3) and CYP75B2 (flavonoid 3’-hydroxylase). Notably, substantial changes were observed in numerous DEGs involved in stress responses, including amino sugar metabolism and the MAPK signaling pathway.

Fig. 6
figure 6

Heat map showed the expression regularity of genes related to stress response under heat stress. The data in the figure are FPKM of DEGs. The color gradient in the heatmap, transitioning from blue to red, signifies a gradual increase in gene expression levels

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Furthermore, after MTS treatment, significant changes occurred in many DEGs associated with plant hormone signaling, including ABA responsive element binding factor (ABF2), Auxin response factor (ARF18), Jasmonic acid-amido synthetase, and Regulatory protein (NPR1) (Fig. 7A and Table S4). To further identify key transcription factors relevant to heat stress tolerance in A. beshanzuensis, we compared the expression profiles of differentially expressed transcription factors following heat stress. Our analysis revealed upregulation of numerous transcription factors such as TIFY6A, SCL9, ARF4, PUB18, IAA13, LAX4, BZR1, and BHLH85 with increasing treatment temperature (Fig. 7B and Table S4). These findings highlight that after high temperature stress, a significant number of stress response genes at the transcriptional level undergo substantial alterations, thereby enhancing heat stress tolerance in A. beshanzuensis.

Fig. 7
figure 7

Heat map showed the expression regularity of genes related to plant hormone transduction signal under heat stress. The data in the figure are FPKM of DEGs. The color gradient in the heatmap, transitioning from blue to red, signifies a gradual increase in gene expression levels

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Discussion

A. beshanzuensis is highly susceptible to severe environmental stresses, particularly elevated temperatures. In recent decades, heat stress induced by global warming and climate change has become an increasingly critical issue affecting plant growth. While extensive research has elucidated the complex mechanisms of heat tolerance in model crops, the physiological and molecular mechanisms underlying the heat tolerance of A. beshanzuensis remain largely unexplored.

Photosynthesis plays a critical physiological role by providing energy and enabling carbon assimilation for plant growth and reproduction [30]. High temperatures adversely affect the photosynthetic system, reducing the rate of carbon assimilation and significantly impacting associated parameters [31]. Our study observed a marked decrease in Yield, ETR, qP, and NPQ values in leaves exposed to high temperatures. These results indicate that elevated temperatures disrupt PSII reaction center activity and hinder electron transfer within thylakoid membrane photosynthetic complexes [32], thereby significantly reducing the photosynthetic rate. Furthermore, under heat stress, the chlorophyll a, chlorophyll b, and total chlorophyll content in leaves decreased significantly. Chlorophyll plays a crucial role in capturing light, facilitating energy transfer, and initiating charge separation during photosynthesis. The decline in chlorophyll content may result from the accumulation of harmful substances within plant cells due to heat stress, which accelerates chlorophyll degradation [33, 34].

Environmental stressors induce a substantial accumulation of ROS in plants, leading to the oxidation of unsaturated fatty acids within cells, increased membrane peroxidation, and subsequent damage to the cellular membrane system and overall cell integrity [35, 36]. Variations in MDA content serve as a reliable indicator for assessing the extent of membrane lipid peroxidation and evaluating membrane damage [37]. Our findings revealed a significant increase in MDA content, indicating extensive damage to the cell membrane caused by elevated temperatures. In response to environmental stress, plants activate antioxidant enzymes such as SOD, POD and CAT to mitigate the harmful effects of ROS [38, 39]. We observed a significant decrease in the activity levels of SOD, POD, and CAT following high-temperature treatment. These findings suggest that the limited heat tolerance of A. beshanzuensis results in cellular damage and structural disruption of key enzymes, ultimately leading to a decline in their activities. Furthermore, our study found a significant decrease in the transcription of antioxidant genes, including GST, GGCT, Mgst3, ND1, COX, and MT-CYB, under elevated temperature conditions. In contrast, previous studies have reported increased transcription of antioxidant genes during environmental stress, contributing to plant resilience [40, 41]. This conflicting result may reflect the susceptibility of A. beshanzuensis to high-temperature stress.

Proline, soluble sugars, and soluble proteins play critical roles as regulators of cellular osmotic pressure and are valuable indicators for assessing stress recovery in plants [42]. Our findings showed that exposure to heat stress significantly increased the levels of proline, soluble sugars, and soluble proteins. This indicates that A. beshanzuensis actively responds to heat stress by enhancing these molecules, mitigating damage, stabilizing biological membranes, and preserving enzymatic activity.

When plants are exposed to external stresses such as heat, cold, and drought, their gene transcription undergoes significant changes. To investigate the molecular basis of heat resistance in A. beshanzuensis, we performed comparative transcriptome analysis under different temperature conditions. Our study revealed that several stress response pathways were inhibited after heat treatment, particularly those involving HSPs such as HSP70, HSP90, and HSPBP1. The HSP family plays a vital role in mitigating heat stress by refolding misfolded proteins or degrading them via ubiquitination-mediated autophagy and the 26 S proteasome system, thus maintaining cellular homeostasis under stress [43, 44]. HSP70, a key stress response protein, is essential for plant stress adaptation [45]. Additionally, upregulation of the HSP90 gene in Arabidopsis and tea plants under various stressors, such as heat, cold, salinity, and heavy metals, underscores its versatile role [44, 46]. HSP70 and HSP90 can form complexes that enhance a plant’s ability to cope with external stresses [47,48,49].

Our observations after heat treatment also revealed increased expression levels of numerous DEGs associated with ABC transporters in the heat-treated samples compared to the control. Under various environmental stresses, heightened expression of ABC transporters is a key mechanism regulating stress tolerance. For instance, overexpression of AtABCG36 in Arabidopsis improved resistance to drought and salinity [50]. Additionally, numerous genes related to the mitogen-activated protein kinase (MAPK) signaling pathway were significantly upregulated following heat stress. Previous studies have shown that ROS accumulation triggers the activation of MAPK signaling cascades, highlighting their role in stress regulation [51]. Flavonoids enhance plant thermotolerance by scavenging ROS to mitigate oxidative stress, stabilizing membrane integrity via lipid peroxidation inhibition, and modulating stress signaling, collectively promoting cellular homeostasis and longevity [52, 53]. Under heat stress, the upregulation of flavonoid biosynthetic genes is generally believed to enhance plant stress tolerance [40, 54]. However, in this study, we observed a significant downregulation of several key flavonoid biosynthetic genes in A. beshanzuensis. This finding suggests that, under high-temperature conditions, A. beshanzuensis may lack the regulatory mechanisms required to initiate or sustain flavonoid biosynthesis, resulting in insufficient thermotolerance. We therefore hypothesize that this species exhibits specific regulatory defects within the flavonoid biosynthetic pathway. Further molecular and biochemical investigations are warranted to elucidate the intrinsic regulatory network underlying its differential heat tolerance.

Excessive ROS accumulation also activates plant hormone signaling pathways, coordinating stress responses [55, 56]. Many DEGs linked to hormone signaling pathways, such as ABF, ARF, GH, BZR, and NPR, exhibited significant changes. Plant hormones regulate growth and development under stress, enhancing tolerance [57, 58]. Brassinosteroids (BRs) are essential plant hormones that regulate various aspects of plant growth and development [59]. BRs not only increase plant tolerance to high temperatures but also enhance BR-induced heat stress tolerance through the overexpression of BZR1 [60]. In soybean, gene expression levels in the JA defense pathway were significantly upregulated following high-temperature and low-light treatments, indicating a responsive adaptation to heat stress [61]. Furthermore, temperature stress activates numerous genes involved in abscisic acid biosynthesis, underscoring their critical role in enhancing heat tolerance [62]. Our study revealed a notable increase in the expression of several transcription factors, including ARF19, ARF4, BZR2 and GH, in A. beshanzuensis subjected to heat stress. These findings, consistent with previous research, indicate that heat stress activates plant hormone signaling pathways, thereby improving plant resilience to adverse conditions. Remarkably, A. beshanzuensis appears to enhance its resistance to heat stress by activating its antioxidant system and hormone signaling pathways, utilizing its distinctive metabolic processes. These results emphasize the pivotal role of genes associated with antioxidant systems and plant hormone signaling pathways in augmenting the heat tolerance of A. beshanzuensis.

Conclusion

To understand how A. beshanzuensis responded to heat stress and the mechanisms contributing to its endangerment, we conducted physiological and transcriptomic analyses under both control and heat stress conditions. Compared to the control group, the high temperature stress groups (MHS and MTS) showed a significant reduction in photosynthetic rate and chlorophyll content, accompanied by notable increases in the activities of MDA, SOD, POD, and CAT enzymes, as well as levels of soluble sugar, soluble protein, and free proline. Transcriptomic analysis indicated the down-regulation of nearly all DEGs associated with photosynthesis. Most DEGs encoding heat shock proteins were up-regulated, highlighting the critical role of sHSPs in A. beshanzuensis response to high temperature stress. Additionally, after MTS treatment, we observed the upregulation of numerous genes linked to plant hormone signaling, suggesting potential activation of this pathway to enhance heat stress tolerance. In summary, this study laid the foundation for further understanding the molecular mechanisms underlying heat resistance in hawthorn and the mechanisms contributing to its susceptibility under heat stress.

Data availability

The sequenced original reads are stored in the National Center for Biotechnology Information Database (NCBI) with entry number PRJNA1064174.

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Acknowledgements

We appreciate the support provided by Baishanzu National Park.

Funding

The authors are grateful for the financial support provided by the Baishanzu National Park Research Project (2023JBGS02 and 2021ZDZX04).

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Author notes

  1. Likang Zhao and Tao Li contributed equally to this work and are joint first authors.

Authors and Affiliations

  1. College of Life Science, Zhejiang Province Key Laboratory of Plant Secondary Metabolism and Regulation, Zhejiang Sci-Tech University, Hangzhou, 310018, China

    Likang Zhao, Tao Li, Zhen Pang & Hongfei Lu

  2. Qianjiangyuan-Baishan National Park Qinyuan Conservation Center, Qingyuan, 323800, China

    Xiaorong Chen, Rongguang Lan, Sumei Wu, Yanyun Xiong, Yiqing Wu & Yougui Wu

  3. College of Life Science, Zhejiang University, Hangzhou, 310058, China

    Mingjian Yu

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Contributions

L.Z., H.L. and M.Y. designed the experiments; T.L. conducted the experiments with the help of X.C., R.L., Z.P. and S.W.; L.Z. and T.L. wrote the paper; Y.X., Y.W., and Y.W. helped to analyze the data and contributed to supervise this study. All authors have approved this manuscript.

Corresponding authors

Correspondence to Hongfei Lu or Mingjian Yu.

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The experimental materials used in this study were provided by Baishanzu National Park. All experimental procedures were carried out in strict accordance with local and national regulations.

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Zhao, L., Li, T., Chen, X. et al. Resistance mechanism of Abies beshanzuensis under heat stress was elucidated through the integration of physiological and transcriptomic analyses. BMC Plant Biol 25, 621 (2025). https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s12870-025-06641-4

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BMC Plant Biology

ISSN: 1471-2229

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