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Article

Comparative Analysis of Mesocotyl Elongation Ability among Maize Inbred Lines

by
Daxing Wen
,
Xiaoyu Tian
,
Chenglai Wu
and
Chunqing Zhang
*
Agronomy College, Shandong Agricultural University, Tai’an 271018, China
*
Author to whom correspondence should be addressed.
Int. J. Mol. Sci. 2024, 25(22), 12437; https://doi.org/10.3390/ijms252212437
Submission received: 19 October 2024 / Revised: 12 November 2024 / Accepted: 17 November 2024 / Published: 19 November 2024
(This article belongs to the Special Issue Plant Physiology and Molecular Nutrition)
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Abstract

:
Mesocotyl plays a key role in the seedling emergence of maize; however, the mechanism of mesocotyl elongation is still unclear. Moreover, different maize inbred lines and cultivars have varied mesocotyl lengths positively correlated with deep sowing tolerance. In this study, we selected one inbred line with long mesocotyl (LM) and two maize inbred lines with short mesocotyl (SM1 and SM2) from more than 400 maize inbred lines. The mesocotyl length of the LM line was about three-fold longer than those of the SM1 and SM2 lines. Microstructure observation showed that the reason for short mesocotyl in the SM1 and SM2 lines was few cell numbers and short cell length, respectively. Subsequently, we used RNA-seq to investigate the mechanism of mesocotyl elongation by regulating cell number and cell length at the transcriptome level. Compared with the LM line, the SM1 line displayed stronger downregulation of Cytochrome P450 and peroxidase genes than the SM2 line. Moreover, plant hormone signal transduction plays a vital role in mesocotyl elongation. Taken together, we propose a model for mesocotyl elongation of maize inbred lines with different cell lengths and cell numbers, which provide new insights into mesocotyl elongation in maize.

1. Introduction

Mesocotyl is an important organ between the coleoptile node and the basal part of the seminal root in Gramineae, which plays a crucial role in the seedling emergence of maize, sorghum, and rice [1,2]. Arabidopsis mainly depends on hypocotyl elongation during seedling emergence [3]. The process of seedling emergence involves transitioning from skotomorphogenesis to photomorphogenesis [4]. Mesocotyl elongation usually occurs in the skotomorphogenesis stage in the soil layer. Numerous studies have revealed the mechanism of hypocotyl elongation; however, the mechanism of mesocotyl elongation is still unclear.
Deep sowing, a method commonly used in arid soils, can significantly induce mesocotyl elongation of maize with deep sowing tolerance [5]. Proper deep sowing can effectively alleviate the damage to maize seedlings caused by drought and low-temperature stress, which is an important measure to avoid drought and cold at the seedling stage [6]. Maize is usually sown to a depth of about 5 cm, while deep sowing can stimulate seed using water from the deep soil to germinate [5]. The mesocotyl length of maize materials with deep sowing tolerance is much longer than that of maize materials sensitive to deep sowing, and the mesocotyl length is significantly positively correlated with deep sowing tolerance [2]. Many studies have shown that mesocotyl elongation is the main reason for maize deep sowing tolerance [7]. Moreover, coleoptile elongation is also a driving force of maize seedlings under deep sowing, but the mesocotyl is more critical than the coleoptile elongation [8,9].
Different maize inbred lines and cultivars have varied mesocotyl lengths because of the genetic diversity of maize. Seedling emergence is fast and uniform in maize materials with long mesocotyl. Under drought stress during the sowing period of maize, appropriately increasing the sowing depth can help the seeds absorb more soil water and promote seed germination and seedling establishment [5]. The mesocotyl length is closely related to the seedling emergence rate [7]. However, maize materials with short mesocotyl are sensitive to deep sowing, failing to break through the soil layer and decreasing seedling emergence rate [10]. Therefore, revealing the mechanism of mesocotyl elongation is of great importance for ensuring rapid and uniform seedling emergence.
Mesocotyl length is a quantitative trait controlled by multiple genes. Many mesocotyl length or deep sowing tolerance-related QTL loci are mapped using GWAS and QTL in maize and rice [1,2,7,8,11]. Under 10 cm and 20 cm sowing depth, deep sowing tolerance-related QTL loci are mapped to chromosomes 1, 3, 4, 6, 7, and 10 in maize by the F2 population constructed with maize inbred lines 3681-4 and X178 [2]. Moreover, 33 QTLs involved in deep sowing tolerance of maize are identified by composite interval mapping, and 50 candidate genes are predicted using RNA-seq data [6]. Using a DH population constructed by B73 and Mo17, a previous study identified 13 QTLs related to mesocotyl length, explaining 2.5–7.8% of phenotypic variance [8]. The QTL regions that have been reported are extensive, indicating that fine mapping with larger populations and more precise and accurate phenotypes is necessary [12]. Many mesocotyl length or deep sowing tolerance-related QTL loci have been identified; however, gene cloning and functional verification involved in maize mesocotyl elongation are still very limited. In particular, the key genes determining mesocotyl length in maize are unknown. It might be possible to mine some genes related to the regulation of mesocotyl elongation based on multi-omics techniques, such as transcriptome and proteome analysis.
Besides genetic factors, mesocotyl elongation is also influenced by environmental conditions and plant hormones [4,13,14]. Mesocotyl elongation is inhibited under light and promoted significantly in darkness [15]. Polyamine oxidase (PAO) activity in maize mesocotyl increases under light, leading to cell wall hardening and inhibiting mesocotyl elongation [16]. The optimum temperature promotes mesocotyl elongation, but neither high nor low temperature is conducive to mesocotyl elongation [12]. Mesocotyl tissue is more vulnerable to low-temperature stress than other tissues during maize seed germination. Therefore, mesocotyl tissue can be used to evaluate the cold tolerance of maize [17]. Mesocotyl elongation is regulated by many plant hormones, such as Indole-3-acetic acid (IAA), cytokinin (CK), gibberellin (GA), abscisic acid (ABA), ethylene (ETH), brassinosteroid (BR), strigolactones (SLs), and jasmonic acid (JA) [9,10]. Plant hormones generally control mesocotyl elongation by regulating cell division or elongation [18]. Various plant hormones regulate rice mesocotyl elongation through complex regulatory pathways [12]. Maize mesocotyl elongation requires both IAA and BR, and BR inhibitors weaken mesocotyl elongation [13,19,20]. The network of plant hormones regulating maize mesocotyl elongation remains ambiguous.
This study aimed to investigate the differences in mesocotyl elongation among maize inbred lines with various mesocotyl lengths at the transcriptome level. We first selected one inbred line with long mesocotyl (LM) and two maize inbred lines with short mesocotyl (SM1 and SM2) from more than 400 maize inbred lines for transcriptome analysis. The reason for short mesocotyl in SM1 and SM2 was a few cell numbers and short cell lengths, respectively. Subsequently, we used RNA-seq to analyze the samples at germination 5 d under dark conditions when mesocotyl grew rapidly. We propose a possible network of mesocotyl elongation of maize inbred lines with different cell lengths and cell numbers, which provide new insights into mesocotyl elongation in maize.

2. Results

2.1. Few Cell Numbers and Short Cell Length Are the Key Factors of Short Mesocotyl Length in Maize

Light can inhibit mesocotyl elongation. To investigate the potential of mesocotyl elongation, we detected the mesocotyl length of more than 400 maize inbred lines after germination 7 d under dark conditions. The results showed that mesocotyl length significantly differed among these inbred lines at germination 7 d (Figure 1A). Paraffin sectioning displayed short mesocotyl length due to few cell numbers or short cell lengths (Figure 1B). In exploring the reasons for short mesocotyl due to few cell numbers, we wanted to exclude or decrease the effects of the cell length. In contrast, the effects of the cell number were eliminated or reduced when we explored the reasons for short mesocotyl due to short cell lengths. Therefore, screening suitable materials was difficult and was needed to measure the numerous materials. Subsequently, we selected one inbred line with long mesocotyl (LM) and two maize inbred lines with short mesocotyl (SM1 and SM2) for transcriptome analysis. The mesocotyl length of the LM line was about three-fold longer than those of the SM1 and SM2 lines (Figure 1C). The SM1 line had a similar cell length compared with the LM line, but the cell number of the SM1 line was remarkably fewer than that in the LM line (Figure 1D,E). There was no significant difference in cell number between the SM2 and LM lines. However, the SM2 line displayed a notably shorter cell length than the LM line. The cells of mesocotyl in the SM2 line were thicker than the LM and SM1 lines (Figure 1B), but the length of mesocotyl is more important for seedlings breaking through the soil layer than the thickness of mesocotyl. Thus, we did not focus on the thickness of mesocotyl. In the subsequent study, we used the SM1 line compared with the LM line (SM1vsLM) and the SM2 line compared with the LM line (SM2vsLM) to investigate the mechanism of mesocotyl elongation by regulating cell number and cell length, respectively.

2.2. Transcriptome Analysis of Mesocotyl Elongation

To explore the regulation network of mesocotyl elongation of maize inbred lines with different cell lengths and cell numbers, we performed transcriptome analysis on samples at germination 5 d under dark conditions when mesocotyl grew rapidly. Mesocotyl samples of three maize inbred lines (LM, SM1, and SM2) with three biological replicates were used for RNA-seq, which generated about 61.45–66.96 million raw reads for each sample (Supplementary Table S1). Then, adapters and sequences with low-quality regions were removed, with nearly 57.42–64.67 million clean reads remaining. About 49.24–58.28 million clean reads were mapped to the maize genome. The clean reads included 83.75%–88.73% uniquely mapped reads and 1.90%–2.09% multiple mapped reads. Subsequently, the DESeq2 R package (1.20.0) was used to identify differentially expressed genes (DEGs) by using adjusted p <0.05 and |log2Foldchange| ≥ 1 as the cutoff. The results showed that 3587 genes were notably upregulated and 4644 genes were significantly downregulated in SM1vsLM. Moreover, 4338 genes were remarkably upregulated and 3690 genes were markedly downregulated in SM2vsLM.

2.3. Many Cytochrome P450 and Peroxidase-Related Genes Were Downregulated in the Short Mesocotyl Lines Compared with the Long Mesocotyl Line

To further understand the function of these DEGs, we performed a Gene Ontology (GO) term enrichment analysis in two comparisons of SM1vsLM and SM2vsLM. The results showed that all the significantly enriched GO terms of the upregulated DEGs in SM1vsLM belonged to the molecular function group, in which the most significantly enriched GO term was oxidoreductase activity (acting on paired donors, GO: 0016705, p = 3.20 × 10−6) (Figure 2A). For the downregulated DEGs in SM1vsLM, there were four significantly enriched GO terms in the cellular component group and nine significantly enriched GO terms in the molecular function group (Figure 2B). Cell wall (GO: 0005618, p = 7.36 × 10−4) belonged to the cellular component group and included 20 downregulated DEGs that were annotated xyloglucan endotransglucosylase/hydrolase protein, pectinesterase, or pectinesterase inhibitor (Table 1). For the upregulated DEGs in SM2vsLM, there were 17 significantly enriched GO terms in the biological process group and 16 significantly enriched GO terms in the molecular function group, with only one significantly enriched GO term in the cellular component group (Figure 2C). Among them, the most significantly enriched GO term was iron ion binding (GO: 0005506, p = 4.97 × 10−11) in the molecular function group. All the significantly enriched GO terms of the downregulated DEGs in SM2vsLM belonged to the molecular function group (Figure 2D). To understand which GO terms might decrease mesocotyl length, we focus on the downregulated GO terms in SM1vsLM and SM2vsLM. Interestingly, the top three significantly enriched GO terms in SM1vsLM were similar to those in SM2vsLM (Figure 2B,D), that is tetrapyrrole binding (GO: 0046906), hydrolase activity (GO: 0004553) and heme binding (GO: 0020037). Moreover, the DEGs in tetrapyrrole binding (GO: 0046906) were the same as heme binding (GO: 0020037) in SM2vsLM, and tetrapyrrole binding (GO: 0046906) had one more DEG than heme binding (GO: 0020037) in SM1vsLM. In the two GO terms, approximately 60% of DEGs were annotated Cytochrome P450, and about 30% of DEGs were annotated peroxidase. Some DEGs were exhibited in both SM1vsLM and SM2vsLM, while other DEGs were exhibited in only SM1vsLM or SM2vsLM (Figure 3). Hydrolase activity (GO: 0004553) displayed various hydrolase-related genes, including some cell wall metabolism-related genes.

2.4. Plant Hormone Signal Transduction-Related Genes Are Involved in Regulating the Length and Number of Mesocotyl Cell

To identify the metabolic pathways involved in mesocotyl elongation, we further analyzed the Kyoto Encyclopedia of Genes and Genomes (KEGG) enrichment pathways. The top two pathways were phenylpropanoid biosynthesis and flavonoid biosynthesis in both SM1vsLM and SM2vsLM, which might play important roles in mesocotyl elongation (Figure 4). Moreover, stilbenoid, diarylheptanoid, gingerol biosynthesis, starch and sucrose metabolism, alpha-linolenic acid metabolism, and plant hormone signal transduction were also significantly enriched in the two comparisons. Numerous studies have reported that many plant hormone-related genes participate in Arabidopsis hypocotyl elongation and mesocotyl elongation in rice and maize [1,3,9,10]. Therefore, we further analyzed the DEGs in the plant hormone signal transduction pathway. The results showed that approximately half of the DEGs in the plant hormone signal transduction pathway were involved in auxin signal transduction, followed by abscisic acid, ethylene, cytokinin, brassinosteroid, and gibberellin signal transduction in SM1vsLM and SM2vsLM (Figure 5). In auxin signal transduction pathway, three auxin influx carrier (AUX1 LAX family) genes (Zm00001d028401, Zm00001d030310, and Zm00001d053004) were downregulated in SM2vsLM, in which Zm00001d028401 and Zm00001d030310 were also downregulated in SM1vsLM. In abscisic acid signal transduction, three abscisic acid receptor PYR/PYL family genes (Zm00001d028793, Zm00001d043014, and Zm00001d047037) were downregulated in SM2vsLM, in which Zm00001d028793 and Zm00001d043014 were also downregulated in SM1vsLM. All four DEGs (Zm00001d014613, Zm00001d026250, Zm00001d005293, and Zm00001d019696) in brassinosteroid signal transduction pathway were downregulated in both SM1vsLM and SM2vsLM. However, one DEG (Zm00001d013412) annotated Arabidopsis histidine kinase 2/3/4 (cytokinin receptor) in cytokinine signal transduction was downregulated only in SM1vsLM. One DEG (Zm00001d043247) annotated ethylene receptor, and three DEGs (Zm00001d022530, Zm00001d050861, and Zm00001d003451) annotated ethylene-insensitive protein. Three were upregulated only in SM2vsLM.

2.5. Validation of RNA-Seq Data

To validate the DEGs identified using RNA-seq, we randomly selected Zm00001d019414 (CYP450) and Zm00001d007161 (Peroxidase) from Figure 3, Zm00001d030310 (Auxin influx carrier) and Zm00001d013412 (Cytokinin receptor) from Figure 5, and Zm00001d046492 (Elongated mesocotyl 2) and Zm00001d029906 (Beta expansin 7) from other DEGs to perform quantitative real-time PCR (qRT-PCR) analyses. The results displayed that the expression patterns of these genes in the qRT-PCR assays were similar to those transcript abundance changes identified by transcriptome analyses (Supplementary Figure S1). Moreover, we selected another maize inbred line with long mesocotyl (B73), two maize inbred lines with long cells and few cell numbers in mesocotyl (NH60 and Lx9801), and two maize inbred lines with short cell and many cell numbers in mesocotyl (HY4 and HB089) to detect the expression level of the above six genes. NH60 and Lx9801 had relatively short mesocotyl mainly due to few cell numbers; however, the cell lengths might also be different compared with LM and B73 (Supplementary Figure S2). Although HY4 and HB089 showed short mesocotyl mainly due to short cells, the cell numbers might also be different compared with LM and B73 (Supplementary Figure S2). The qRT-PCR results showed that the newly selected maize inbred lines displayed similar expression patterns with the maize inbred lines in transcriptome analyses (Figure 6). The above results indicated that the RNA-seq data were reliable.

3. Discussion

Under dark conditions, the growth of maize mesocotyl shows a slow-fast-slow trend, along with significant changes in the contents of auxin, cellulose, and POD activity [21]. The POD activity of mesocotyl is notably increased in light than in darkness [15]. Under the condition of no control of light, skotomorphogenesis, and photomorphogenesis affected the mesocotyl elongation together. Therefore, the mechanism of mesocotyl elongation under no control of light was very complicated. To eliminate the influence of light on mesocotyl elongation, we evaluated maize mesocotyl length via germination under dark conditions to explore the mechanism of mesocotyl elongation in maize. Moreover, we found many DEGs annotated Cytochrome P450 and peroxidase were downregulated in both SM1vsLM and SM2vsLM (Figure 3). Cytochrome P450 family genes in plants are involved in various physiological processes, such as plant metabolism, stress responses, phytohormones, and signaling molecules [22,23]. POD is an essential enzyme in lignin metabolism related to maize mesocotyl elongation [24]. Therefore, Cytochrome P450 and peroxidase genes might play important roles in mesocotyl elongation in maize.
A previous study identified three xyloglucan endotransglucosylase/hydrolase genes regulating mesocotyl elongation in sorghum based on transcriptome analysis [25]. In this study, we found that 13 DEGs annotated xyloglucan endotransglucosylase/hydrolases were downregulated in SM1vsLM by GO enrichment analysis. These results indicated that xyloglucan endotransglucosylase/hydrolases might play important roles in the mesocotyl elongation of maize and sorghum.
Many plant hormones regulate mesocotyl elongation in maize and rice and hypocotyl elongation in Arabidopsis. Plant hormones affect mesocotyl length by regulating cell number and cell length [12]. The primary source of IAA in mesocotyl is the coleoptile unit (including the primary leaf and coleoptile segment), and more than 50% of IAA comes from the coleoptile tip [26]. The IAA content in the epidermis irradiated by red light is lower than that of the control in darkness [27,28]. The growth rate of mesocotyl at 20 cm depth is 1.5–2 times that at 2 cm depth, mainly due to the regulation of the rapid elongation of mesocotyl by increasing IAA synthesis and transport [29]. In this study, different maize inbred lines showed significant differences in mesocotyl length, and the expression levels of three AUX1 genes encoding auxin influx carrier in the auxin signal transduction pathway were downregulated in short mesocotyl maize inbred lines, indicating that auxin plays a vital role in the rapid elongation of mesocotyl.
ABA promotes the growth of rice mesocotyl by prolonging the cell division activity of meristem, and fluridone (FLU, an inhibitor of ABA biosynthesis) inhibits mesocotyl elongation [30]. BR can promote mesocotyl elongation by inhibiting the phosphorylation of U-type cyclin CYC U2 by OsGSK2 [1]. Moreover, 2.0 mg/L exogenous 24-epibrassinolide significantly increased the mesocotyl length of maize [9]. In this study, the expression of ABA receptor PYR/PYL family genes and TCH4 and CYCD3 genes in the BR signal transduction pathway were downregulated in short mesocotyl maize inbred lines, indicating that ABA and BR promote mesocotyl elongation, which is consistent with previous studies.
The antagonism of CK and SLs regulates the elongation of rice mesocotyl in the dark, and d10-1 and d14-1 mutants are more sensitive to CK than the wild type [31]. In this study, the cytokinin receptor CRE1 gene was downregulated only in maize inbred line SM1 with few mesocotyl cell numbers, indicating that cytokinin signaling regulates mesocotyl cell number.
Ethephon and coronatine can decrease mesocotyl length by inhibiting cell elongation in maize [32]. Ethylene-insensitive protein 3 (EIN3) in the ethylene signal transduction pathway slows down the elongation of hypocotyl cells in Arabidopsis by activating the ERF1 pathway [3]. In this study, the expression levels of ethylene receptor ETR and EIN3 genes in the ethylene signal transduction pathway were only upregulated in maize inbred line SM2 with short mesocotyl cell length, indicating that they might play an important role in inhibiting mesocotyl elongation in maize, similar to the results in Arabidopsis.
Maize mesocotyl elongation is more sensitive to GA3 under 20 cm sowing depth than under 2 cm sowing depth [33]. Moreover, exogenous GA promotes mesocotyl elongation under deep sowing conditions [34]. Gene chip analysis and exogenous GA processing showed that ZmMYB59 responded to deep sowing through the GA signaling pathway in maize [35]. Dynamic transcriptome and plant hormone analysis of rice mesocotyl elongation in response to light showed that light reduced the contents of IAA and GA3 and increased JA levels to inhibit mesocotyl elongation [36]. In this study, compared with the DEGs in other plant hormone signal transduction pathways, maize inbred lines with different mesocotyl lengths had the fewest DEGs in GA signal transduction pathways, and the degree of upregulation and downregulation was also relatively low. The results indicate that GA signal transduction might not be the main reason for varied mesocotyl length in this study.
Taken together, we propose a possible network of mesocotyl elongation of maize inbred lines with different cell lengths and cell numbers (Figure 7). Compared with the maize inbred line with long mesocotyl, the maize inbred line with few cell number of mesocotyl displayed stronger downregulation of Cytochrome P450 and peroxidase genes than the maize inbred line with short cell length of mesocotyl. Moreover, plant hormone signal transduction plays important roles in mesocotyl elongation, in which AUX1, PRY/PRL, TCH4, and CYCD3 genes involved in auxin, abscisic acid, and brassinosteroid signal transduction are downregulated in the maize inbred lines with few cell number or short cell length of mesocotyl. Notably, CRE1 in cytokinin signal transduction is downregulated only in the maize inbred line with few cell numbers of mesocotyl. However, ETR and EIN3 genes related to ethylene signal transduction are upregulated only in the maize inbred line with a short cell length of mesocotyl. The expression levels of the above genes might determine mesocotyl length.

4. Materials and Methods

4.1. Materials

To investigate the differences in mesocotyl elongation among maize inbred lines with long and short mesocotyl, we selected three maize inbred lines (LM, SM1, and SM2) with different mesocotyl lengths from more than 400 maize inbred lines. Moreover, another maize inbred line with long mesocotyl (B73), two maize inbred lines with long cells and few cell numbers in mesocotyl (NH60 and Lx9801), and two maize inbred lines with short cells and many cell numbers in mesocotyl (HY4 and HB089) to validate RNA-seq data. These maize inbred lines were grown at the experimental station of Shandong Agricultural University (36°90′ N and 117°90′ E, Tai’an City, Shandong Province, China). The newly harvested seeds were used for subsequent experiments.

4.2. Measurement of Mesocotyl Length

Maize seeds were sown in a sprouting bed consisting of silica sand with 60% saturation moisture content at 1 cm sowing depth in a germination box. Then, the seeds were kept at 25 ± 1 °C in darkness for seven days. After washing silica sand from maize seedlings, mesocotyl length was measured by a ruler. The mean of about 30 mesocotyl length represented the mesocotyl length per replicate. Each maize inbred line included three replicates.

4.3. Measurement of Cell Length and Cell Number of Mesocotyl

Cell length and cell number in a vertical line of mesocotyl were measured by microstructure observation according to a previous study with minor modifications [37]. Approximately 1 cm of the middle part of mesocotyl was immersed in 50% formalin–acetic acid–alcohol (FAA) fixative. Paraffin sectioning and histological staining were performed by a previous study [37]. The longitudinal sections of the middle part of mesocotyl were observed by a microscope. Cell length was measured from the mean length of 10 randomly selected cells per sample. In the longitudinal section of mesocotyl, meristematic cells, rapidly growing cells, and mature cells are located in the 1.0 mm, 3.0 mm, and 5.0 mm zones below the mesocotyl node, respectively [38]. In this study, the apical meristematic part and the rapid elongation part are much shorter (about 0.5 cm) compared to the middle elongation part and the lower mature part at germination 7 d under dark conditions. Thus, the cell number in a vertical line of mesocotyl was calculated by dividing the mesocotyl length into cell length.

4.4. RNA-Seq and Transcriptome Analysis

Mesocotyl samples from 30 seedlings at germination 5 d under dark conditions were pooled together as one biological replicate. Each treatment included three biological replicates. Mesocotyl samples were frozen in liquid nitrogen and then kept at −80 °C until RNA extraction. Frozen samples were ground by using a ball mill. The ground samples (approximately 0.1 g) were used for total RNA extraction by the RNA extraction kit DP441 (Tiangen, Beijing, China). RNA integrity and concentration were examined as previously described [39]. RNA-seq library construction and sequencing were conducted according to a previous study [40]. Raw reads produced from RNA-seq were preprocessed to obtain clean reads, and then they were mapped to the maize reference genome sequence (B73 v4, ftp.ensemblgenomes.org/pub/plants/release-47/fasta/zea_mays/dna/ accessed on 10 October 2024) by using HISAT2. Feature Counts (v1.5.0-p3) were used to count the number of reads mapped to each gene. Differential expression analysis of two groups was analyzed by using the DESeq2 R package (1.20.0) [41]. Then, the p values were adjusted according to the Benjamini and Hochberg algorithm. Differentially expressed genes (DEGs) were identified by using adjusted p < 0.05 and |log2Foldchange| ≥ 1 as the cutoff. Gene Ontology (GO) enrichment analysis and Kyoto Encyclopedia of Genes and Genomes (KEGG) pathways enrichment analysis were performed as previously described [40].

4.5. qRT-PCR

The qRT-PCR assays were performed according to a previous study [39]. Primer 6 software was used to design gene-specific primers, which are listed in Supplementary Table S2. A PrimeScript RT reagent kit (Takara, Dalian, China) was applied to synthesize cDNA. All qRT-PCR assays were repeated at least three times. The maize Actin gene (Zm00001d010159) was used as an internal control to normalize the expression levels of the selected genes. The primers of the Actin gene came from a previous study [42]. The relative expression levels of genes were calculated by using the 2−ΔΔCt method [43].

4.6. Statistical Analysis

We used SPSS 19.0 software (SPSS, Chicago, IL, USA) to perform statistical analysis.

5. Conclusions

The reason for short mesocotyl in the SM1 and SM2 lines was a few cell numbers and short cell lengths, respectively. Transcriptome analysis revealed that Cytochrome P450, peroxidase genes, and plant hormone signal transduction pathway play important roles in mesocotyl elongation. Taken together, we propose a model of mesocotyl elongation among maize inbred lines with different cell lengths and cell numbers, which provide new insights into mesocotyl elongation in maize.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/ijms252212437/s1.

Author Contributions

D.W. and C.Z. designed the study. D.W. and X.T. performed most of the experiments and analyzed the results. C.W. contributed to materials and field experiments. C.Z. supervised this study. D.W. and C.Z. wrote the manuscript. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Natural Science Foundation of Shandong Province (ZR2021QC139), the National Natural Science Foundation of China (32272092), and the Modern Agricultural Industry Technology System Innovation Team of Shandong Province (SDAIT-02-02).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Data are contained within the article and Supplementary Materials.

Conflicts of Interest

The authors declare no conflicts of interest.

References

  1. Sun, S.; Wang, T.; Wang, L.; Li, X.; Jia, Y.; Liu, C.; Huang, X.; Xie, W.; Wang, X. Natural selection of a GSK3 determines rice mesocotyl domestication by coordinating strigolactone and brassinosteroid signaling. Nat. Commun. 2018, 9, 2523. [Google Scholar] [CrossRef] [PubMed]
  2. Zhang, H.; Ma, P.; Zhao, Z.; Zhao, G.; Tian, B.; Wang, J.; Wang, G. Mapping QTL controlling maize deep-seeding tolerance-related traits and confirmation of a major QTL for mesocotyl length. Theor. Appl. Genet. 2012, 124, 223–232. [Google Scholar] [CrossRef] [PubMed]
  3. Zhong, S.; Shi, H.; Xue, C.; Wei, N.; Guo, H.; Deng, X.W. Ethylene-orchestrated circuitry coordinates a seedling’s response to soil cover and etiolated growth. Proc. Natl. Acad. Sci. USA 2014, 111, 3913–3920. [Google Scholar] [CrossRef] [PubMed]
  4. Leivar, P.; Monte, E.; Oka, Y.; Liu, T.; Carle, C.; Castillon, A.; Huq, E.; Quail, P.H. Multiple Phytochrome-Interacting bHLH Transcription Factors Repress Premature Seedling Photomorphogenesis in Darkness. Curr. Biol. 2008, 18, 1815–1823. [Google Scholar] [CrossRef] [PubMed]
  5. Sáenz Rodríguez, M.N.; Cassab, G.I. Primary Root and Mesocotyl Elongation in Maize Seedlings: Two Organs with Antagonistic Growth below the Soil Surface. Plants 2021, 10, 1274. [Google Scholar] [CrossRef]
  6. Zhao, X.; Niu, Y.; Hossain, Z.; Shi, J.; Mao, T.; Bai, X. Integrated QTL Mapping, Meta-Analysis, and RNA-Sequencing Reveal Candidate Genes for Maize Deep-Sowing Tolerance. Int. J. Mol. Sci. 2023, 24, 6770. [Google Scholar] [CrossRef]
  7. Yang, Y.; Ma, Y.; Liu, Y.; Lyle, D.; Li, D.; Wang, P.; Xu, J.; Zhen, S.; Lu, J.; Peng, Y.; et al. Dissecting the genetic basis of maize deep-sowing tolerance by combining association mapping and gene expression analysis. J. Integr. Agric. 2022, 21, 1266–1277. [Google Scholar] [CrossRef]
  8. Liu, H.; Zhang, L.; Wang, J.; Li, C.; Zeng, X.; Xie, S.; Zhang, Y.; Liu, S.; Hu, S.; Wang, J.; et al. Quantitative Trait Locus Analysis for Deep-Sowing Germination Ability in the Maize IBM Syn10 DH Population. Front. Plant Sci. 2017, 8, 813. [Google Scholar] [CrossRef]
  9. Zhao, X.; Zhong, Y.; Zhou, W. Molecular mechanisms of mesocotyl elongation induced by brassinosteroid in maize under deep-seeding stress by RNA-sequencing, microstructure observation, and physiological metabolism. Genomics 2021, 113, 3565–3581. [Google Scholar] [CrossRef]
  10. Chen, F.; Ji, X.; Bai, M.; Zhuang, Z.; Peng, Y. Network Analysis of Different Exogenous Hormones on the Regulation of Deep Sowing Tolerance in Maize Seedlings. Front. Plant Sci. 2021, 12, 739101. [Google Scholar] [CrossRef]
  11. Liu, H.; Zhan, J.; Li, J.; Lu, X.; Liu, J.; Wang, Y.; Zhao, Q.; Ye, G. Genome-Wide Association Study (GWAS) for Mesocotyl Elongation in Rice (Oryza sativa L.) under Multiple Culture Conditions. Genes 2020, 11, 49. [Google Scholar] [CrossRef] [PubMed]
  12. Zhan, J.; Lu, X.; Liu, H.; Zhao, Q.; Ye, G. Mesocotyl elongation, an essential trait for dry-seeded rice (Oryza sativa L.): A review of physiological and genetic basis. Planta 2020, 251, 27. [Google Scholar] [CrossRef] [PubMed]
  13. Kutschera, U.; Wang, Z. Growth-limiting proteins in maize coleoptiles and the auxin-brassinosteroid hypothesis of mesocotyl elongation. Protoplasma 2016, 253, 3–14. [Google Scholar] [CrossRef]
  14. Zhang, D.; Jing, Y.; Jiang, Z.; Lin, R. The Chromatin-Remodeling Factor PICKLE Integrates Brassinosteroid and Gibberellin Signaling during Skotomorphogenic Growth in Arabidopsis. Plant Cell 2014, 26, 2472–2485. [Google Scholar] [CrossRef]
  15. Zhao, X.; Niu, Y.; Hossain, Z.; Zhao, B.; Bai, X.; Mao, T. New insights into light spectral quality inhibits the plasticity elongation of maize mesocotyl and coleoptile during seed germination. Front. Plant Sci. 2023, 14, 1152399. [Google Scholar] [CrossRef] [PubMed]
  16. Cona, A.; Cenci, F.; Cervelli, M.; Federico, R.; Mariottini, P.; Moreno, S.; Angelini, R. Polyamine Oxidase, a Hydrogen Peroxide-Producing Enzyme, Is Up-Regulated by Light and Down-Regulated by Auxin in the Outer Tissues of the Maize Mesocotyl. Plant Physiol. 2003, 131, 803–813. [Google Scholar] [CrossRef]
  17. Gao, C.; Hu, J.; Zhang, S.; Zheng, Y.; Knapp, A. Association of polyamines in governing the chilling sensitivity of maize genotypes. Plant Growth Regul. 2009, 57, 31–38. [Google Scholar] [CrossRef]
  18. Xiong, Q.; Ma, B.; Lu, X.; Huang, Y.; He, S.; Yang, C.; Yin, C.; Zhao, H.; Zhou, Y.; Zhang, W.; et al. Ethylene-Inhibited Jasmonic Acid Biosynthesis Promotes Mesocotyl/Coleoptile Elongation of Etiolated Rice Seedlings. Plant Cell 2017, 29, 1053–1072. [Google Scholar] [CrossRef]
  19. Hartwig, T.; Corvalan, C.; Best, N.B.; Budka, J.S.; Zhu, J.; Choe, S.; Schulz, B. Propiconazole is a specific and accessible brassinosteroid (BR) biosynthesis inhibitor for Arabidopsis and maize. PLoS ONE 2012, 7, e36625. [Google Scholar] [CrossRef]
  20. Hu, S.; Sanchez, D.L.; Wang, C.; Lipka, A.E.; Yin, Y.; Gardner, C.A.C.; Lübberstedt, T. Brassinosteroid and gibberellin control of seedling traits in maize (Zea mays L.). Plant Sci. 2017, 263, 132–141. [Google Scholar] [CrossRef]
  21. Niu, L.; Wu, Z.; Liu, H.; Wu, X.; Wang, W. 2-DE-based proteomic analysis of protein changes associated with etiolated mesocotyl growth in Zea mays. BMC Genom. 2019, 20, 758. [Google Scholar] [CrossRef] [PubMed]
  22. Li, Y.; Wei, K. Comparative functional genomics analysis of cytochrome P450 gene superfamily in wheat and maize. BMC Plant Biol. 2020, 20, 93. [Google Scholar] [CrossRef] [PubMed]
  23. Hansen, C.C.; Nelson, D.R.; Møller, B.L.; Werck-Reichhart, D. Plant cytochrome P450 plasticity and evolution. Mol. Plant 2021, 14, 1244–1265. [Google Scholar] [CrossRef] [PubMed]
  24. Zhao, X.; Niu, Y.; Bai, X.; Mao, T. Transcriptomic and Metabolic Profiling Reveals a Lignin Metabolism Network Involved in Mesocotyl Elongation during Maize Seed Germination. Plants 2022, 11, 1034. [Google Scholar] [CrossRef]
  25. Ju, L.; Lv, N.; Yin, F.; Niu, H.; Yan, H.; Wang, Y.; Fan, F.; Lv, X.; Chu, J.; Ping, J. Identification of Key Genes Regulating Sorghum Mesocotyl Elongation through Transcriptome Analysis. Genes 2023, 14, 1215. [Google Scholar] [CrossRef]
  26. Iino, M.; Carr, D.J. Sources of Free IAA in the Mesocotyl of Etiolated Maize Seedlings. Plant Physiol. 1982, 69, 1109–1112. [Google Scholar] [CrossRef]
  27. Fellner, M.; Ford, E.D.; Volkenburgh, E.V. Development of Erect Leaves in a Modern Maize Hybrid is Associated with Reduced Responsiveness to Auxin and Light of Young Seedlings in vitro. Plant Signal. Behav. 2006, 1, 201–211. [Google Scholar] [CrossRef]
  28. Jones, A.M.U.O.; Cochran, D.S.; Lamerson, P.M.; Evans, M.L.; Cohen, J.D. Red light-regulated growth. I. Changes in the abundance of indoleacetic acid and a 22-kilodalton auxin-binding protein in the maize mesocotyl. Plant Physiol. 1991, 97, 352–358. [Google Scholar] [CrossRef]
  29. Zhao, G.; Wang, J. Effect of auxin on mesocotyl elongation of dark-grown maize under different seeding depths. Russ. J. Plant Physiol. 2010, 57, 79–86. [Google Scholar] [CrossRef]
  30. Watanabe, H.; Takahashi, K.; Saigusa, M. Morphological and anatomical effects of abscisic acid (ABA) and fluridone (FLU) on the growth of rice mesocotyls. Plant Growth Regul. 2001, 34, 273–275. [Google Scholar] [CrossRef]
  31. Hu, Z.; Yamauchi, T.; Yang, J.; Jikumaru, Y.; Tsuchida-Mayama, T.; Ichikawa, H.; Takamure, I.; Nagamura, Y.; Tsutsumi, N.; Yamaguchi, S.; et al. Strigolactone and Cytokinin Act Antagonistically in Regulating Rice Mesocotyl Elongation in Darkness. Plant Cell Physiol. 2014, 55, 30–41. [Google Scholar] [CrossRef] [PubMed]
  32. Liu, Y.; Zhou, Y.; Huang, G.; Zhu, N.; Li, Z.; Zhang, M.; Duan, L. Coronatine inhibits mesocotyl elongation by promoting ethylene production in etiolated maize seedlings. Plant Growth Regul. 2020, 90, 51–61. [Google Scholar] [CrossRef]
  33. Zhao, G.C.A.U.; Wang, J. Effect of gibberellin and uniconazole on mesocotyl elongation of dark-grown maize under different seeding depths. Plant Prod. Sci. 2008, 11, 423–429. [Google Scholar] [CrossRef]
  34. Pan, B.; Zhong, T.; Zhao, G. Promoting deep-sowing germinability of corn (Zea mays) by seed soaking with gibberellic acid. Arch. Agron. Soil Sci. 2017, 63, 1314–1323. [Google Scholar] [CrossRef]
  35. Du, L.; Jiang, H.; Zhao, G.; Ren, J. Gene cloning of ZmMYB59 transcription factor in maize and its expression during seed germination in response to deep-sowing and exogenous hormones. Plant Breed. 2017, 136, 834–844. [Google Scholar] [CrossRef]
  36. Feng, F.; Mei, H.; Fan, P.; Li, Y.; Xu, X.; Wei, H.; Yan, M.; Luo, L. Dynamic transcriptome and phytohormone profiling along the time of light exposure in the mesocotyl of rice seedling. Sci. Rep. 2017, 7, 11961. [Google Scholar] [CrossRef]
  37. Xie, L.; Wen, D.; Wu, C.; Zhang, C. Transcriptome analysis reveals the mechanism of internode development affecting maize stalk strength. BMC Plant Biol. 2022, 22, 49. [Google Scholar] [CrossRef]
  38. Niu, L.; Hao, R.; Wu, X.; Wang, W. Maize mesocotyl: Role in response to stress and deep-sowing tolerance. Plant Breed. 2020, 139, 466–473. [Google Scholar] [CrossRef]
  39. Wen, D.; Xu, H.; Xie, L.; He, M.; Hou, H.; Wu, C.; Li, Y.; Zhang, C. Effects of Nitrogen Level during Seed Production on Wheat Seed Vigor and Seedling Establishment at the Transcriptome Level. Int. J. Mol. Sci. 2018, 19, 3417. [Google Scholar] [CrossRef]
  40. Meng, A.; Wen, D.; Zhang, C. Dynamic Changes in Seed Germination under Low-Temperature Stress in Maize. Int. J. Mol. Sci. 2022, 23, 5495. [Google Scholar] [CrossRef]
  41. Love, M.I.; Huber, W.; Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014, 15, 550. [Google Scholar] [CrossRef] [PubMed]
  42. Zhang, Z.; Yang, J.; Wu, Y. Transcriptional Regulation of Zein Gene Expression in Maize through the Additive and Synergistic Action of opaque2, Prolamine-Box Binding Factor, and O2 Heterodimerizing Proteins. Plant Cell 2015, 27, 1162–1172. [Google Scholar] [CrossRef] [PubMed]
  43. Livak, K.J.; Schmittgen, T.D. Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT method. Methods 2001, 25, 402–408. [Google Scholar] [CrossRef] [PubMed]
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Figure 1. Phenotypes of three maize inbred lines: (A) Mesocotyl at germination 7 d under dark conditions, scale bar represents 1 cm, arrows indicate the coleoptile nodes; (B) Images of the vertical section of the center of mesocotyl, scale bars represent 100 μm; (C) Mesocotyl length; (D) Mesocotyl cell length; (E) Mesocotyl cell number in a vertical line. LM is a maize inbred line with long cells and many cell numbers in mesocotyl. SM1 is a maize inbred line with long cells and few cell numbers in mesocotyl. SM2: a maize inbred line with short cell and many cell numbers in mesocotyl. Error bars display the standard deviation for three replicates. Different letters show significant differences among treatments (p-value < 0.05).
Figure 1. Phenotypes of three maize inbred lines: (A) Mesocotyl at germination 7 d under dark conditions, scale bar represents 1 cm, arrows indicate the coleoptile nodes; (B) Images of the vertical section of the center of mesocotyl, scale bars represent 100 μm; (C) Mesocotyl length; (D) Mesocotyl cell length; (E) Mesocotyl cell number in a vertical line. LM is a maize inbred line with long cells and many cell numbers in mesocotyl. SM1 is a maize inbred line with long cells and few cell numbers in mesocotyl. SM2: a maize inbred line with short cell and many cell numbers in mesocotyl. Error bars display the standard deviation for three replicates. Different letters show significant differences among treatments (p-value < 0.05).
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Figure 2. Significantly enriched Gene Ontology (GO) terms: (A) GO terms for the upregulated genes in SM1vsLM. (B) GO terms for the downregulated genes in SM1vsLM. (C) GO terms for the upregulated genes in SM2vsLM. (D) GO terms for the downregulated genes in SM2vsLM. GO terms were sorted based on p-values. LM is a maize inbred line with long cells and many cell numbers in mesocotyl. SM1 is a maize inbred line with long cells and few cell numbers in mesocotyl. SM2: a maize inbred line with short cell and many cell numbers in mesocotyl.
Figure 2. Significantly enriched Gene Ontology (GO) terms: (A) GO terms for the upregulated genes in SM1vsLM. (B) GO terms for the downregulated genes in SM1vsLM. (C) GO terms for the upregulated genes in SM2vsLM. (D) GO terms for the downregulated genes in SM2vsLM. GO terms were sorted based on p-values. LM is a maize inbred line with long cells and many cell numbers in mesocotyl. SM1 is a maize inbred line with long cells and few cell numbers in mesocotyl. SM2: a maize inbred line with short cell and many cell numbers in mesocotyl.
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Figure 3. Heat map of selected DEGs annotated Cytochrome P450 and peroxidase from GO terms for the downregulated genes in SM1vsLM and SM2vsLM. LM is a maize inbred line with long cells and many cell numbers in mesocotyl. SM1 is a maize inbred line with long cells and few cell numbers in mesocotyl. SM2: a maize inbred line with short cell and many cell numbers in mesocotyl. The × represents that it is not a DEG in the comparison.
Figure 3. Heat map of selected DEGs annotated Cytochrome P450 and peroxidase from GO terms for the downregulated genes in SM1vsLM and SM2vsLM. LM is a maize inbred line with long cells and many cell numbers in mesocotyl. SM1 is a maize inbred line with long cells and few cell numbers in mesocotyl. SM2: a maize inbred line with short cell and many cell numbers in mesocotyl. The × represents that it is not a DEG in the comparison.
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Figure 4. Top 20 Kyoto Encyclopedia of Genes and Genomes (KEGGs) pathways in SM1vsLM and SM2vsLM. LM is a maize inbred line with long cells and many cell numbers in mesocotyl. SM1 is a maize inbred line with long cells and few cell numbers in mesocotyl. SM2: a maize inbred line with short cell and many cell numbers in mesocotyl.
Figure 4. Top 20 Kyoto Encyclopedia of Genes and Genomes (KEGGs) pathways in SM1vsLM and SM2vsLM. LM is a maize inbred line with long cells and many cell numbers in mesocotyl. SM1 is a maize inbred line with long cells and few cell numbers in mesocotyl. SM2: a maize inbred line with short cell and many cell numbers in mesocotyl.
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Figure 5. Heat map of selected DEGs from the plant hormone signal transduction pathway in SM1vsLM and SM2vsLM. LM is a maize inbred line with long cells and many cell numbers in mesocotyl. SM1 is a maize inbred line with long cells and few cell numbers in mesocotyl. SM2: a maize inbred line with short cell and many cell numbers in mesocotyl. The × represents that it is not a DEG in the comparison.
Figure 5. Heat map of selected DEGs from the plant hormone signal transduction pathway in SM1vsLM and SM2vsLM. LM is a maize inbred line with long cells and many cell numbers in mesocotyl. SM1 is a maize inbred line with long cells and few cell numbers in mesocotyl. SM2: a maize inbred line with short cell and many cell numbers in mesocotyl. The × represents that it is not a DEG in the comparison.
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Figure 6. Validation of the expression levels of DEGs in more maize inbred lines using qRT-PCR. Red bars represent the maize inbred lines with long mesocotyl. Green bars represent the maize inbred lines with long cells and few cell numbers in mesocotyl. Blue bars represent the maize inbred lines with short cells and many cell numbers in mesocotyl. Error bars represent the standard deviation for three replicates.
Figure 6. Validation of the expression levels of DEGs in more maize inbred lines using qRT-PCR. Red bars represent the maize inbred lines with long mesocotyl. Green bars represent the maize inbred lines with long cells and few cell numbers in mesocotyl. Blue bars represent the maize inbred lines with short cells and many cell numbers in mesocotyl. Error bars represent the standard deviation for three replicates.
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Figure 7. A possible network of mesocotyl elongation of maize inbred lines with different cell lengths and cell numbers. The red and green arrows indicate upregulated and downregulated genes, respectively. The thickened green arrow means stronger downregulation. LM is a maize inbred line with long cells and many cell numbers in mesocotyl. SM1 is a maize inbred line with long cells and few cell numbers in mesocotyl. SM2: a maize inbred line with short cell and many cell numbers in mesocotyl. AUX1: auxin influx carrier (AUX1 LAX family). PYR/PYL: abscisic acid receptor PYR/PYL family. TCH4: xyloglucan:xyloglucosyl transferase TCH4. CYCD3: cyclin D3. CRE1: cytokinin receptor. ETR: ethylene receptor. EIN3: ethylene-insensitive protein 3.
Figure 7. A possible network of mesocotyl elongation of maize inbred lines with different cell lengths and cell numbers. The red and green arrows indicate upregulated and downregulated genes, respectively. The thickened green arrow means stronger downregulation. LM is a maize inbred line with long cells and many cell numbers in mesocotyl. SM1 is a maize inbred line with long cells and few cell numbers in mesocotyl. SM2: a maize inbred line with short cell and many cell numbers in mesocotyl. AUX1: auxin influx carrier (AUX1 LAX family). PYR/PYL: abscisic acid receptor PYR/PYL family. TCH4: xyloglucan:xyloglucosyl transferase TCH4. CYCD3: cyclin D3. CRE1: cytokinin receptor. ETR: ethylene receptor. EIN3: ethylene-insensitive protein 3.
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Table 1. DEGs in the cell wall GO term in SM1vsLM.
Table 1. DEGs in the cell wall GO term in SM1vsLM.
Gene IDGene Annotationlog2FoldChangep-Value
Zm00001d044775Xyloglucan endotransglucosylase/hydrolase protein 3−9.427.18 × 10−14
Zm00001d026250Xyloglucan endotransglucosylase/hydrolase protein 24−5.924.22 × 10−4
Zm00001d051526Probable xyloglucan endotransglucosylase/hydrolase protein 30−5.658.86 × 10−4
Zm00001d026251Probable xyloglucan endotransglucosylase/hydrolase protein 16−4.871.52 × 10−2
Zm00001d024378Xyloglucan endotransglucosylase/hydrolase 2−4.772.05 × 10−11
Zm00001d050201Probable xyloglucan endotransglucosylase/hydrolase protein 25−3.913.85 × 10−4
Zm00001d002409Probable xyloglucan endotransglucosylase/hydrolase protein 16−3.806.49 × 10−3
Zm00001d009899Probable pectinesterase/pectinesterase inhibitor 41−3.544.49 × 10−10
Zm00001d022104Pectinesterase QRT1−3.472.28 × 10−8
Zm00001d024392Probable xyloglucan endotransglucosylase/hydrolase protein 25−3.071.88 × 10−3
Zm00001d053961Probable xyloglucan endotransglucosylase/hydrolase protein 30−3.026.85 × 10−3
Zm00001d032992Pectinesterase 31−2.271.24 × 10−49
Zm00001d047970Probable xyloglucan endotransglucosylase/hydrolase protein 28−2.012.98 × 10−22
Zm00001d045048Probable pectinesterase/pectinesterase inhibitor 12−1.833.38 × 10−53
Zm00001d002412Probable xyloglucan endotransglucosylase/hydrolase protein 25−1.692.74 × 10−3
Zm00001d042624Probable pectinesterase/pectinesterase inhibitor 51−1.393.49 × 10−36
Zm00001d012766Probable pectinesterase 53−1.317.44 × 10−9
Zm00001d042625Probable pectinesterase/pectinesterase inhibitor 51−1.227.04 × 10−28
Zm00001d014613Xyloglucan endotransglucosylase/hydrolase protein 22−1.171.43 × 10−21
Zm00001d021667Probable xyloglucan endotransglucosylase/hydrolase protein 8−1.071.86 × 10−20
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Wen, D.; Tian, X.; Wu, C.; Zhang, C. Comparative Analysis of Mesocotyl Elongation Ability among Maize Inbred Lines. Int. J. Mol. Sci. 2024, 25, 12437. https://doi.org/10.3390/ijms252212437

AMA Style

Wen D, Tian X, Wu C, Zhang C. Comparative Analysis of Mesocotyl Elongation Ability among Maize Inbred Lines. International Journal of Molecular Sciences. 2024; 25(22):12437. https://doi.org/10.3390/ijms252212437

Chicago/Turabian Style

Wen, Daxing, Xiaoyu Tian, Chenglai Wu, and Chunqing Zhang. 2024. "Comparative Analysis of Mesocotyl Elongation Ability among Maize Inbred Lines" International Journal of Molecular Sciences 25, no. 22: 12437. https://doi.org/10.3390/ijms252212437

APA Style

Wen, D., Tian, X., Wu, C., & Zhang, C. (2024). Comparative Analysis of Mesocotyl Elongation Ability among Maize Inbred Lines. International Journal of Molecular Sciences, 25(22), 12437. https://doi.org/10.3390/ijms252212437

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