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Article

Comparative Transcriptomic Analysis Reveals the Involvement of Auxin Signaling in the Heat Tolerance of Pakchoi under High-Temperature Stress

by
Bing Yang
1,2,†,
Yaosong Chen
1,†,
Xiaofeng Li
1,
Lu Gao
1,
Liming Miao
1,
Yishan Song
2,
Dingyu Zhang
1,* and
Hongfang Zhu
1,*
1
Shanghai Key Laboratory of Protected Horticultural Technology, Horticultural Research Institute, Shanghai Academy of Agricultural Sciences, Shanghai 201403, China
2
College of Food Science and Technology, Shanghai Ocean University, Shanghai 201306, China
*
Authors to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Agronomy 2024, 14(8), 1604; https://doi.org/10.3390/agronomy14081604
Submission received: 28 May 2024 / Revised: 9 July 2024 / Accepted: 11 July 2024 / Published: 23 July 2024
(This article belongs to the Special Issue Metabolomics-Centered Mining of Crop Metabolic Diversity and Function)
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Versions Notes

Abstract

:
Pakchoi is a kind of nonheading Chinese cabbage being widely cultivated not only in China but also all over Asia. High temperature is a major limiting factor influencing the yield and quality of pakchoi, while the mechanism of pakchoi dealing with high-temperature challenges remains largely elusive. In the present study, we conducted a comparative transcriptomic analysis, which was also validated by qPCR, of the heat-tolerant Xinxiaqing (XXQ) variant and Suzhouqing (SZQ) variant, which are heat-sensitive under high-temperature treatment. Gene Ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) analyses suggest that high-temperature-induced phytohormones signal transduction, especially auxin signal transduction, regulates the heat responses of pakchoi. Our further investigations imply that high-temperature-activated auxin signal plays a positive role in helping pakchoi deal with high-temperature challenge; IAA-pretreated pakchoi plants exhibited greater resistance to the high-temperature treatment, probably due to the induction of antioxidant activity. In addition, our study also identified six heat shock proteins/factors (HSPs/HSFs) whose up-regulation correlates with the elevated heat tolerance of pakchoi. Notably, among these high-temperature-induced heat-responsive factors, HSP20 and HSP26.5 are under the regulation of auxin signal, and this signal cascade contributes to enhancing the thermostability of pakchoi. In the present study, we identified crucial high-temperature-responsive factors and signaling pathways in pakchoi, which help in understanding the mechanism of pakchoi coping with high-temperature challenge.

1. Introduction

Pakchoi, a kind of nonheading Chinese cabbage, is an important vegetable crop being widely cultivated all over Asia [1]. Pakchoi is a cool-loving crop, which prefers to grow in cool climates [2]; the global greenhouse effect inevitably causes extremely high-temperature climates and this usually leads to a great loss of pakchoi production [3]. Elevated temperature has been identified as the most detrimental environmental factor with far-reaching implications on plant development and growth [4]. In summer, the sweltering weather poses a significant threat to pakchoi by inducing growth stunting and leaving indelible damage on the leaves, thereby impacting overall production [5,6].
The mechanisms underlying the recognition of high temperature by plants and how high-temperature-induced signals transduce to regulate gene expression are important topics in plant–environment interactions [7,8]. Under high-temperature threat, plants undergo profound remodeling at both physiological and molecular levels to retain internal homeostasis, thus supporting survival [9,10]. High-temperature stress invokes intricate alterations, including in the stability of the genome, signal transduction pathways, epigenetic regulation, and the modulation of heat shock proteins (HSPs) in plants [11,12,13,14]. Heat shock factors (HSFs) constitute the primary regulatory module in plants under high-temperature stress [15]. The expression of HSPs is controlled and regulated by HSFs [16]. In response to elevated temperature, plants accumulate HSFs, which subsequently trigger the expression of HSPs as well as many other stress-related genes, ultimately improving the thermal tolerance of plants [17,18,19]. Many HSPs act as molecular chaperones to influence protein folding and aggregation, thereby maintaining protein homeostasis and cellular stabilization, which contribute to the survival ability of plants under heat stress [20]. However, the current research on pakchoi, as well as on other Brassica rapa species, is far from comprehensive and has left critical gaps in understanding their thermal tolerance mechanisms.
Phytohormones play a pivotal role in orchestrating plant responses to various abiotic stresses [21]. Previous research has revealed the involvement of phytohormones such as abscisic acid (ABA) and jasmonic acid (JA) in regulating the responses of plants to drought, high-temperature, and salinity stresses [22,23,24]. Recent advances have extended our understanding of auxin, which is mainly regarded as a key regulatory factor in regulating plant growth and development, in the complex mechanism underlying plants’ response to abiotic stresses [25,26]. It was reported that exogenous IAA application, or the genetic manipulation of auxin biosynthesis and signaling, helps to alleviate drought- and heat-induced spikelet sterility and stabilize grain yield in Oryza sativa [27]. Phytochrome-interacting factor 4 (PIF4) acts as a crucial player in the heat response pathway [28]. Intriguingly, PIF4 also mediates auxin signaling to facilitate the thermomorphogenesis of plants [29]. In addition, auxin also crosstalks with other signals, such as reactive oxygen species (ROS), in regulating plants to deal with abiotic stresses, and many auxin-responsive genes are also regulated by ROS [30].
Despite these advances, the intricacies of how auxin operates in mediating pakchoi adaptation to high-temperature challenges remain elusive. In the present study, we analyzed the physiological and molecular differences between a heat-tolerant and a heat-sensitive cultivar. Through transcriptome analysis, we investigated the molecular basis underlying the difference between these two cultivars in response to high temperature. Our results highlight that auxin signal contributes to the elevation of thermostability in pakchoi, during which auxin-regulated HSP20 and antioxidant activity may play crucial roles. Our results not only provide important clues in revealing the mechanism of pakchoi adapting to high-temperature stress but also enrich our understanding of the function of auxin in pakchoi.

2. Materials and Methods

2.1. Plant Materials and Growth Conditions

In this study, we used two cultivars to investigate the mechanism of heat tolerance in pakchoi. Xinxiaqing (abbreviated as XXQ), which was previously created by us with high thermostability and mainly cultivated in Shanghai now, is stored in our laboratory at the Horticultural Research Institute, Shanghai Academy of Agricultural Sciences. Suzhouqing (abbreviated as SZQ) is a common cultivar widely cultivated in China, with a heat-sensitive character. Plant materials were cultured in an incubator (Yanghui, Ningbo, China) under a 16:8 h light/dark photoperiod, with a light intensity of approximately 60 µmol m−2 s−1, cultivation temperature of 22 °C, and 60% humidity.

2.2. High-Temperature Treatment of Pakchoi

Pakchoi seeds were sown in a 108-hole tray to initiate germination. After reaching the two-true-leaf stage, pakchoi seedlings were transferred into pots for further growth. After emerging 5–6 true leaves, high-temperature treatment (42 °C) was implemented on pakchoi plants for 0 h, 6 h, 12 h, or 2 days, as described in the figure legends. After high-temperature treatment, pakchoi plants and leaves were harvested for the subsequent analyses.

2.3. Measurement of FV/FM

Leaves from the same position of XXQ and SZQ plants were selected and subjected to measurement of maximum photochemical efficiency (FV/FM) of photosystem II (PSII). In brief, leaves were placed under darkness for about half an hour and then FV/FM of leaves was detected with a calibrated chlorophyll fluorescence imaging system (WALZ IMAG-MAX/L, Nuremberg, Germany).

2.4. Measurement of Relative Moisture Content

Detached leaves from the same position of XXQ and SZQ plants were collected following high-temperature treatment. Briefly, the fresh weight of leaf samples was recorded as FW. Then, samples were soaked in distilled water at room temperature of 25 °C for 5–7 h, the swelling weight of leaf samples measured, and it was recorded as TW. Drying the leaf samples in a 72 °C oven for 48 h, the dry weight was obtained and recorded as DW.
Leaf water content was calculated using the following equation:
RWC (%) = (FW − DW)/(T − DW) × 100; the moisture content in the control sample was arbitrarily set to 1 after being calculated.

2.5. Measurement of Antioxidant Activities and Protein Content

POD, CAT, and SOD activities and protein content were determined by the detection kits (Comin, Item No. POD-1-Y, CAT-1-W, SOD-1-W, BCAP-1-W, Suzhou, China) according to the manufacturer’s instructions.

2.6. Total RNA Extraction, Library Construction, and Sequencing

RNA extraction, library construction, and subsequent transcriptome sequencing were facilitated by the services of Shanghai Majorbio Bio-Pharm Technology Co., Ltd. (Shanghai, China). Chinensis (Cultivar NHCC001) v1.0 Genome (Download Detail (njau.edu.cn)) was used as the referenced genome. The DESeq2 (3.19) was used for differential expression analysis. Genes with a cut-off value of log2 (fold change) ≥ 1 and adjusted p-value < 0.05 were defined as DEGs. Gene Ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) enrichment analyses were conducted on https://cloud.majorbio.com/page/tools/ (accessed on 15 October 2023).

2.7. IAA Treatment of Pakchoi

For IAA inducing pakchoi thermostability examination, living plants were pretreated with 250 μm/L IAA (Shanghai yuanye Bio-Technology Co., Ltd., Shanghai, China) solution via spraying and water-treated plants were used as controls. After 6 h IAA and water treatments, pakchoi plants were subjected to high-temperature treatment and samples were harvested two days post treatment for further analyses.

2.8. qRT-PCR Analysis

RNA was reverse transcribed into cDNA using the PrimeScript RT Master Mix Kit (Takara, Beijing, China). The 20 µL qPCR reaction solution entailed 1 µL (200 ng/μL) of cDNA, 1 µL each of upstream and downstream primers, 0.4 µL of Passive Reference Dye II, and 10 µL of TransStart Top Green qPCR SuperMix (TransGen Biotech, Beijing, China), with the volume brought up to 20 µL with ddH2O. Primers were synthesized by Qingke Biotechnology Co., Ltd (Beijing, China). The relative expression level of genes was calculated utilizing the 2−ΔΔCt primers listed in Table S2.

3. Results

3.1. Analysis of Phenotypic Differences between the High-Temperature-Tolerant and Sensitive Materials in Response to Heat Treatment

To explore the mechanism of heat tolerance in pakchoi, we conducted phenotypic and physiological analyses on the heat-tolerant XXQ cultivar, which we bred before, and the heat-sensitive SZQ cultivar under high-temperature treatment. As shown in Figure 1, high-temperature treatment seriously damaged the phenotypic and physiological statuses of SZQ (Figure 1A,B), and a great decline in photosynthetic function in its leaves was detected after high-temperature treatment (Figure 1C,D); we also examined the water content and the result shows that high temperature led to rapid water loss in leaves of SZQ (Figure 1E). Meanwhile, in the heat-tolerant XXQ cultivar, high-temperature damages were significantly weaker compared with those in SZQ (Figure 1A–E, Figure S1 and S2).

3.2. Analysis of High-Temperature Treatment-Induced Alterations in Transcriptomes of XXQ and SZQ

As 6 h high-temperature treatment is sufficient to induce phenotypic differences between XXQ and SZQ, we further analyzed the transcriptomic alteration of 6 h high-temperature-treated XXQ and SZQ leaves. Initial transcriptome data underwent a cleansing process, etc., yielding clean 6.02 Gb reads. Aligning the curated reads with a reference genome resulted in a comparability range, which varied from 79.72% to 91.41% (Table S1; Figure S3). Principal component analysis (PCA) implies a good repeatability in each group, and the high-temperature-treated samples significantly differed from the control samples; the transcriptomes of XXQ and SZQ leaves also showed an obvious difference before high-temperature treatment (Figure 2A). Following high-temperature challenge, the transcriptome of XXQ leaves was perturbed involving 4113 up-regulated and 4360 down-regulated genes; in the transcriptome of SZQ leaves, 3692 and 3769 genes responded to high-temperature treatment, being up- and down-regulated, respectively (Figure 2B–E). Collectively, these findings provide molecular evidence of the considerable differences exhibited between XXQ and SZQ in response to high-temperature treatment.

3.3. Identification of Molecular Signaling Pathway Correlated with High-Temperature Tolerance of Pakchoi

Considering the inherent genetic variations distinguishing XXQ from SZQ, we subsequently focused on dissecting the discrepant gene expression patterns initiated by high temperature between these two cultivars (Figure S4). Under high-temperature treatment, 2783 genes were up-regulated and 2843 genes were down-regulated specifically in XXQ but not in SZQ (Figure 3A,B). GO analysis of these high-temperature-responsive genes that up-regulated specifically in XXQ showed that the strong tolerance of XXQ to high temperature is linked to multiple signaling pathways, including auxin signaling, responses to oxidative and organic substances, hormone-mediated signaling pathways, etc. (Figure 3C). KEGG enrichment analysis suggested that genes up-regulated by high temperature in XXQ were predominantly associated with protein processes in the endoplasmic reticulum, zeatin biosynthesis, plant circadian rhythm, plant hormone signal transduction, and mitogen-activated protein kinase (MAPK) signaling pathway (Figure 3D). GO analysis of the 2843 down-regulated genes specifically in XXQ showed that pathways which are pivotal for the sustenance of basic life operations, such as cytoplasmic translation, glucose metabolism, and photosynthesis, were greatly impaired (Figure 3F). Similarly, KEGG analysis revealed that signaling pathways which govern essential cellular metabolism aspects, such as ribosome, glucosamine biosynthesis, photosynthesis, and carbon fixation in photosynthetic organisms, were suppressed by high-temperature treatment (Figure 3E). Collectively, these results suggest that XXQ enhances its tolerance to high temperature through activating phytohormones and some abiotic-stress-related signaling pathways, meanwhile, inhibit its growth and development by declining photosynthesis and basic metabolic processes.

3.4. Analysis of the Expression Pattern of Phytohormone Signal-Associated Genes between XXQ and SZQ in Response to High-Temperature Treatment

GO and KEGG enrichment analyses both highlighted that phytohormone signaling pathways were noticeably activated in the heat-tolerant XXQ cultivar after high-temperature treatment (Figure 3). Consequently, we further analyzed the expression profiles of genes enriched in the phytohormone signaling pathways that exhibited significant divergence between in XXQ and SZQ. Results showed that two jasmonic acid (JA) pathway components, namely JAR1 and MYC2, exhibited more pronounced up-regulation in XXQ compared with those in SZQ (Figure 4A). In the salicylic acid (SA) pathway, NPR1, TGA6, and TGA7 were markedly up-regulated in XXQ (Figure 4B). The abscisic acid (ABA) receptor protein genes, PYLs and ABI1, presented elevated expression levels in XXQ following high-temperature exposure (Figure 4C). It is noted that, of all the signaling pathways that were activated specifically in XXQ, the auxin signaling pathway stands out and comprises eight IAAs that were substantially up-regulated in XXQ, which highlights the critical role of the auxin signaling pathway in XXQ dealing with high-temperature stress (Figure 4D).

3.5. IAA Promotes the Tolerance of Pakchoi to High-Temperature Treatment

Auxin signaling pathway was predominantly activated specifically in XXQ after high-temperature treatment (Figure 3C); in addition, the expression of a multitude of auxin signaling-pathway-associated genes displayed robust upregulation in XXQ (Figure 4D). Consequently, we examined whether applying IAA could elevate the heat tolerance of pakchoi. The heat-sensitive SZQ was pretreated with exogenous IAA, followed by exposure to high-temperature treatment, with water-pretreated SZQ plants serving as a control. As shown in Figure 5A,B, compared with the control samples, IAA-pretreated SZQ exhibited an appreciably enhanced heat tolerance under high-temperature treatment and IAA treatment effectively relieved the damage induced by high-temperature treatment on SZQ plants and leaves. Examination of FV/FM and chlorophyll content in high-temperature-treated SZQ leaves revealed a significant difference between the IAA-treated and control samples (Figure 5C–E). The antioxidant activities in IAA-pretreated SZQ were also higher than those in the control samples (Figure 5F–H). These results suggest that the high-temperature-induced auxin signaling pathway truly contributes to the heat tolerance of pakchoi.

3.6. Identification of High-Temperature and IAA Inductions Correlated HSFs/HSPs in Pakchoi

Based on the GO and KEGG analysis results, we further dissected the abiotic stress-related pathways induced by high temperature in XXQ (Figure 3). Intriguingly, six HSFs/HSPs, namely HSFA8, HSP20, HSFA1E, HIP1, HSFA7B, and HSFA26.5, exhibited higher expression levels in XXQ compared with those in SZQ; these heat-responsive genes were enriched in response to abiotic stimulus, response to stimulus, and response to oxygen-containing compound pathways (Figure 6A). As high-temperature-induced auxin signal contributes to improving the tolerance of pakchoi, we further examined whether these HSFs/HSPs are under the regulation of IAA. Results showed that only two HSF/HSPs were induced by IAA treatment, and especially HSP20 showed a significant up-regulation under IAA treatment (Figure 6B–G). These results imply that auxin may regulate the expression of HSP20 to mediate the tolerance of pakchoi under high-temperature stress.

4. Discussion

Global warming is an insidious environmental menace, which recurrently causes extreme weather [31]. Elevated temperature, hence, has surfaced as a formidable challenge for plant life, which imposes severe constraints on their growth and development [32]. Much evidence has highlighted that high temperature seriously damages the photosynthetic rate and respiration of green plants [33,34]. Hitherto, a myriad of studies illuminated the molecular module of plants in response to heat treatment and identified numerous heat-stress-induced factors, especially in Arabidopsis thaliana and Oryza sativa [35,36]. These identified factors act as key modulators in activation of heat responses under high-temperature treatment [37]. However, the molecular mechanism of pakchoi in response to heat stress remains elusive. In the present study, we identified 2783 up-regulated and 2843 down-regulated genes that are explicitly regulated by high temperature in the thermotolerant XXQ cultivar (Figure 3A,B). GO and KEGG analyses revealed that these genes were associated with phytohormones (especially auxin)-mediated signaling pathways and some basal cellular-metabolism-maintaining pathways (Figure 3C–F). We also subjected the genes which exhibit a differential expression pattern between XXQ and SZQ before high-temperature treatment to GO and KEGG analyses. The analyses results illuminate that there are inherent differences in the transcriptome of XXQ and SZQ, and these differences involve protein binding, ribosomal structures, and metabolic processes (Figure S4). We propose these differences may contribute to the specific morphology of XXQ and SZQ under normal conditions.
Under high-temperature stress, plants initiate an array of physiological mobilization to adapt and withstand the thermal burden, during which phytohormones play critical roles [38,39]. Previous research found that phytohormones in a lower dose could orchestrate various physiological and biochemical responses to help plants deal with high-temperature stress, and application of exogenous phytohormones on seedlings contributes to improving their heat tolerance [21,40,41]. In the present study, we subjected the high-temperature-regulated differentially expressed genes to GO and KEGG analyses and discovered a marked activation of plant phytohormone signaling pathways in the heat-tolerant XXQ line (Figure 3). Scrutinizing the expression profiles of high-temperature-induced genes in phytohormone signaling pathways demonstrates stark differences between XXQ and SZQ (Figure 4). Notably, several genes exhibit significant expression fluctuation involving the signaling pathways of JA, SA, ABA, and auxin under high-temperature treatment. Particularly, eight auxin-signal-associated genes showed dramatic up-regulation, especially in the heat-tolerant XXQ cultivar after high-temperature treatment (Figure 4). Motivated by these findings, we further verified that exogenous IAA application could enhance the thermotolerance of pakchoi (Figure 5). These findings emphasize the important role of auxin in helping pakchoi deal with high-temperature stress.
HSFs and HSPs are definitively the critical components in regulating the adaptation of plants to heat stress [42]. Transcriptomic investigation on plant seedlings revealed the up-regulation of several HSPs under the induction of heat stress, including HSP17.6A and HSP21 in Arabidopsis, HSP18 in tobacco, and HSP22 and HSP40 in tomato [43,44,45,46,47]. The expressions of HSPs are regulated by the specific type of transcription factors named as HSFs [48]. High temperature results in a higher load of denatured proteins, which leads to the relocation of HSFs into the nucleus, thus activating the expression of HSPs [19]. The thermotolerance-inducing function of HSFs also has been elucidated in numerous plant species, such as HSFA7 in Citrus, HSFA1b in wheat, and HSFA in lily [49,50,51]. In the present study, we identified six HSPs/HSFs, namely HSFA8, HSP20, HSFA1E, HIP1, HSFA7B, and HSP26.5, displaying significant up-regulation, especially in the heat-tolerant XXQ cultivar (Figure 6). Intriguingly, high-temperature-induced auxin signaling did not show an overall induction on these six HSPs/HSFs and exogenous auxin treatment only induced the expression of HSP20 and HSFA26.5 (Figure 6). These observations suggest that high-temperature-responsive JA, SA, IAA, and ABA may also regulate the expression of HSPs/HSFs, so it will be of interest to further investigate the effects of these high-temperature-induced phytohormone signals on pakchoi and the relationships between JA, SA, IAA, ABA, and auxin signals (Figure S5). Even though our study identified auxin signaling and some crucial HSPs and HSFs contributing to the thermostability of pakchoi, our findings revealed important molecular clues underlying the heat tolerance of pakchoi under high-temperature challenge, which will help the molecular breeding of heat-tolerant pakchoi in the future.

5. Conclusions

By conducting a comparative transcriptomic analysis between a heat-tolerant and a heat-sensitive pakchoi cultivar under high temperature, we identified that the activation of auxin signaling corelates with the thermostability of pakchoi; our investigations also imply that auxin-signal-induced antioxidant activity and HSP20 expression contribute to the elevation of heat tolerance of pakchoi. In the future, it is worth creating auxin-signaling-related genetic materials of pakchoi, which would help to further elucidate the mechanism of auxin-signaling-induced thermostability of pakchoi.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/agronomy14081604/s1, Figure S1 SOD and CAT activities in SZQ and XXQ after high-temperature treatment; Figure S2 Protein content and expression level of nitrogen metabolism-related genes in XXQ and SZQ during high-temperature treatment; Figure S3. Comparison of gene expression patterns between RNA-seq and qRT-PCR results; Figure S4. Analysis of the transcriptional differences between XXQ and SZQ under normal conditions; Figure S5 Phytohormone-related gene expression pattern in response to IAA under high-temperature treatment; Table S1. Statistical sequence alignment between our sequencing results and the reference genome (A represents Xinxiaqing, B represents Suzhouqing); Table S2. Primer sequences were used in the present study.

Author Contributions

H.Z. and D.Z. designed the experiment. B.Y., Y.C., L.M., X.L. and L.G. conducted the experiments and analyzed the data. B.Y. and D.Z. wrote the manuscript. Y.S. provided comments on the manuscript. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by the Shanghai Agricultural Science and Technology Innovation Project (grant numbers: K2023015).

Data Availability Statement

The original contributions presented in this study are included in the article/Supplementary Material; further inquiries can be directed to the corresponding authors. Raw data of RNA-seq are available in NCBI Sequence Read Archive (SRA), accession numbers: PRJNA1070993.

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. Analysis of heat tolerance of XXQ and SZQ under high-temperature treatment. (A) Phenotypes of XXQ and SZQ plants after high-temperature treatment; (B) phenotypes of XXQ and SZQ leaves after high-temperature treatment; (C) chlorophyll fluorescence images of XXQ and SZQ leaves after high-temperature treatment; (D) FV/FM of XXQ and SZQ leaves after high-temperature treatment; (E) relative water content of XXQ and SZQ leaves after high-temperature treatment. Processing temperature: 42 °C. Data are means ± SD (n = 3 biological replicates), *** p < 0.001, ** p < 0.01, * p < 0.05 (t-test).
Figure 1. Analysis of heat tolerance of XXQ and SZQ under high-temperature treatment. (A) Phenotypes of XXQ and SZQ plants after high-temperature treatment; (B) phenotypes of XXQ and SZQ leaves after high-temperature treatment; (C) chlorophyll fluorescence images of XXQ and SZQ leaves after high-temperature treatment; (D) FV/FM of XXQ and SZQ leaves after high-temperature treatment; (E) relative water content of XXQ and SZQ leaves after high-temperature treatment. Processing temperature: 42 °C. Data are means ± SD (n = 3 biological replicates), *** p < 0.001, ** p < 0.01, * p < 0.05 (t-test).
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Figure 2. Overview of transcriptomes of XXQ and SZQ leaves in response to high-temperature treatment. (A) PCA of XXQ and SZQ transcriptomes; (B) statistical analysis of differentially expressed genes in XXQ and SZQ leaves before and after high-temperature treatment; (C) volcano plot of differentially expressed genes between XXQ and SZQ leaves before high-temperature treatment; (D) Volcano plot of differentially expressed genes of XXQ leaves before and after high-temperature treatment; (E) volcano plot of differentially expressed genes of SZQ leaves before and after high-temperature treatment. The threshold for defining differentially expressed genes is |Log2Fold Change| ≥ 1, p-value < 0.05; n = 3 biological replicates.
Figure 2. Overview of transcriptomes of XXQ and SZQ leaves in response to high-temperature treatment. (A) PCA of XXQ and SZQ transcriptomes; (B) statistical analysis of differentially expressed genes in XXQ and SZQ leaves before and after high-temperature treatment; (C) volcano plot of differentially expressed genes between XXQ and SZQ leaves before high-temperature treatment; (D) Volcano plot of differentially expressed genes of XXQ leaves before and after high-temperature treatment; (E) volcano plot of differentially expressed genes of SZQ leaves before and after high-temperature treatment. The threshold for defining differentially expressed genes is |Log2Fold Change| ≥ 1, p-value < 0.05; n = 3 biological replicates.
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Figure 3. Analysis of signaling pathways regulated by high temperature specifically in XXQ. (A) Venn diagram of the up-regulated genes between XXQ and SZQ after high-temperature treatment; (B) Venn diagram of the down-regulated genes between XXQ and SZQ after high-temperature treatment; (C,D) GO and KEGG analyses of the differentially expressed genes specifically up-regulated in XXQ after high-temperature treatment; (E,F) KEGG and GO analyses of the differentially expressed genes specifically down-regulated in XXQ; data are means ± SD (n = 3 biological replicates).
Figure 3. Analysis of signaling pathways regulated by high temperature specifically in XXQ. (A) Venn diagram of the up-regulated genes between XXQ and SZQ after high-temperature treatment; (B) Venn diagram of the down-regulated genes between XXQ and SZQ after high-temperature treatment; (C,D) GO and KEGG analyses of the differentially expressed genes specifically up-regulated in XXQ after high-temperature treatment; (E,F) KEGG and GO analyses of the differentially expressed genes specifically down-regulated in XXQ; data are means ± SD (n = 3 biological replicates).
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Figure 4. Expression profile analysis of genes in phytohormone pathways under high-temperature treatment in XXQ and SZQ. (A) Expression profile of JA signaling pathway genes under high-temperature treatment in XXQ and SZQ; (B) expression profile of SA signaling pathway genes under high-temperature treatment in XXQ and SZQ; (C) expression profile of ABA signaling pathway genes under high-temperature treatment in XXQ and SZQ; (D) expression profile of auxin signaling pathway genes under high-temperature treatment in XXQ and SZQ. Data are means of transcripts per million (TPM) ± SD (n = 3 biological replicates), *** p < 0.001, ** p < 0.01, * p < 0.05 (t-test).
Figure 4. Expression profile analysis of genes in phytohormone pathways under high-temperature treatment in XXQ and SZQ. (A) Expression profile of JA signaling pathway genes under high-temperature treatment in XXQ and SZQ; (B) expression profile of SA signaling pathway genes under high-temperature treatment in XXQ and SZQ; (C) expression profile of ABA signaling pathway genes under high-temperature treatment in XXQ and SZQ; (D) expression profile of auxin signaling pathway genes under high-temperature treatment in XXQ and SZQ. Data are means of transcripts per million (TPM) ± SD (n = 3 biological replicates), *** p < 0.001, ** p < 0.01, * p < 0.05 (t-test).
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Figure 5. IAA induces the heat tolerance of SZQ. (A,B) Phenotypes of IAA- and water-treated SZQ plants and leaves after high-temperature treatment; (C) chlorophyll fluorescence images of IAA- and water-treated SZQ leaves after high-temperature treatment; (D) FV/FM of IAA- and water-treated SZQ after high-temperature treatment; (E) chlorophyll content of IAA- and water-treated SZQ after high-temperature treatment. (F) POD activity of IAA- and water-treated SZQ after high-temperature treatment; (G) CAT activity of IAA- and water-treated SZQ after high-temperature treatment; (H) SOD activity of IAA- and water-treated SZQ after high-temperature treatment. Processing time: 2d, temperature: 42 °C, IAA concentration: 250 μM/L. Data are means ± SD (n = 3 biological replicates), *** p < 0.001, ** p < 0.01, * p < 0.05 (t-test).
Figure 5. IAA induces the heat tolerance of SZQ. (A,B) Phenotypes of IAA- and water-treated SZQ plants and leaves after high-temperature treatment; (C) chlorophyll fluorescence images of IAA- and water-treated SZQ leaves after high-temperature treatment; (D) FV/FM of IAA- and water-treated SZQ after high-temperature treatment; (E) chlorophyll content of IAA- and water-treated SZQ after high-temperature treatment. (F) POD activity of IAA- and water-treated SZQ after high-temperature treatment; (G) CAT activity of IAA- and water-treated SZQ after high-temperature treatment; (H) SOD activity of IAA- and water-treated SZQ after high-temperature treatment. Processing time: 2d, temperature: 42 °C, IAA concentration: 250 μM/L. Data are means ± SD (n = 3 biological replicates), *** p < 0.001, ** p < 0.01, * p < 0.05 (t-test).
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Figure 6. Expression patterns of HSFs/HSPs in response to high-temperature and IAA treatments. (A) Heat map of HSFs/HSPs expression, which are related with heat stress in XXQ; (B–G) qPCR result of BraHSFA8, BraHSP20, BraHSP26.5, BraHSFA7B, BraHSFA1E, and BraHIP1 expression level under IAA and water treatments; water treatment was used as a negative control. Processing time: 2d, temperature: 42 °C, IAA concentration: 250 μM/L. Data are means ± SD (n = 3 biological replicates), **** p < 0.0001, * p < 0.05 (t-test). Primers were listed in Table S2.
Figure 6. Expression patterns of HSFs/HSPs in response to high-temperature and IAA treatments. (A) Heat map of HSFs/HSPs expression, which are related with heat stress in XXQ; (B–G) qPCR result of BraHSFA8, BraHSP20, BraHSP26.5, BraHSFA7B, BraHSFA1E, and BraHIP1 expression level under IAA and water treatments; water treatment was used as a negative control. Processing time: 2d, temperature: 42 °C, IAA concentration: 250 μM/L. Data are means ± SD (n = 3 biological replicates), **** p < 0.0001, * p < 0.05 (t-test). Primers were listed in Table S2.
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Yang, B.; Chen, Y.; Li, X.; Gao, L.; Miao, L.; Song, Y.; Zhang, D.; Zhu, H. Comparative Transcriptomic Analysis Reveals the Involvement of Auxin Signaling in the Heat Tolerance of Pakchoi under High-Temperature Stress. Agronomy 2024, 14, 1604. https://doi.org/10.3390/agronomy14081604

AMA Style

Yang B, Chen Y, Li X, Gao L, Miao L, Song Y, Zhang D, Zhu H. Comparative Transcriptomic Analysis Reveals the Involvement of Auxin Signaling in the Heat Tolerance of Pakchoi under High-Temperature Stress. Agronomy. 2024; 14(8):1604. https://doi.org/10.3390/agronomy14081604

Chicago/Turabian Style

Yang, Bing, Yaosong Chen, Xiaofeng Li, Lu Gao, Liming Miao, Yishan Song, Dingyu Zhang, and Hongfang Zhu. 2024. "Comparative Transcriptomic Analysis Reveals the Involvement of Auxin Signaling in the Heat Tolerance of Pakchoi under High-Temperature Stress" Agronomy 14, no. 8: 1604. https://doi.org/10.3390/agronomy14081604

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