As an ancient family of channel proteins, aquaporin protein run through the whole development process of plants and play an important role in coordinating the water relationship among roots, stems, leaves and seeds. In plants, there are abundant types of aquaporin proteins, which are divided into four subfamilies according to their sequence homology, namely plasma intrinsic proteins (PIP), NOD26-like intrinsic protein (NIP), tonoplast intrinsic proteins (TIP), and small alkaline intrinsic protein (SIP) (Sakurai et al., 2005). Among them, PIP subfamily has been widely studied. Maurel et al. (2008) found that the expression of PIPs would not only cause changes in stomatal opening and closing regulation, but also determine the diffusion efficiency of CO₂, H₂O₂, and so on in cells. In addition, most PIP genes are expressed in leaves, and their expression is regulated by development. The PIPs expression positions of C₃ plants and C₄ plants are very different in leaves. The PIPs of C₃ plants, such as rice, barley, and tobacco, are highly expressed in mesophyll cells (Heinen et al., 2009). Among them, the high expression of rice in mesophyll cells maintained the water potential and contributed to the diffusion of CO₂ in mesophyll. After overexpression of OsPIP1, the biomass of it was significantly higher than that of normal plants, one of the reasons was that it increased the assimilation rate of CO₂ in mesophyll cells (Sakurai et al., 2008). Tobacco aquaporin protein is involved in the growth of mesophyll cells and promotes the gas exchange between mesophyll cells and the atmosphere (Siefritz et al., 2004). Different from C₃ plants, some PIPs of C₄ plant maize were highly expressed in vascular sheath cells, and participated in the water drainage of xylem vascular sheath. The heterologous expression of ZmPIP1 in yeast showed that it not only promoted the transmembrane diffusion, but also participated in the permeation of CO₂ (Heinen et al., 2009).

Aquaporin proteins are essential for the movement of H₂O, CO₂, and other polar small molecules within and outside the biofilm, and their regulated expression characteristics are closely related to photosynthesis (Maurel et al., 2008). CO₂ and H₂O are important raw materials for plant photosynthesis, and simple diffusion in plants alone will not be enough to maintain photosynthesis (Li et al., 2015). Studies have shown that aquaporin proteins has higher CO₂ and H₂O transfer efficiency, which changes the composition of membrane lipids and increases their solubility on the membrane, thus affecting photosynthesis (Yang and Cui, 2009). In photosynthesis, C₄ plants have higher photosynthetic efficiency than C₃ plants, which is related to the specific cell structure of C₄ plant leaves in morphology. Previous studies have shown that the presence of specific vascular sheath cells in C₄ plants is one of the reasons for the difference in photosynthetic efficiency (Maai et al., 2011). There are two kinds of cells in the leaves of C₄ maize: vascular sheath cells and mesophyll cells. CO₂ in the atmosphere is immobilized in mesophyll cells and converted into malic acid under the action of malic dehydrogenase. Malic acid is transported to the bundle sheath cells for decarboxylation, and the CO₂ released is re fixed by Calvin cycle, thus forming the unique CO₂ pump of C₄ plants, which improves the efficiency of photosynthesis. In contrast, photosynthesis in C₃ plants occurs only in mesophyll cells. Sade et al. (2015) found that after silencing the aquaporin protein of bundle sheath, the hydraulic conductivity of the plant in the bundle sheath cell decreased, indicating that the water in the bundle sheath was transported by the aquaporin protein. Bundle sheath cells sense the pressure signal in xylem sap and affect the hydraulic conduction through the wall of xylem, and then regulate the activity of aquaporin in bundle sheath cells by changing cell osmotic pressure.

Photosynthesis of plants is highly dynamic, which is strongly dependent on environmental conditions and regulated by environmental conditions and endogenous states. The diurnal cycle is an important environmental control factor. It controls the daily and seasonal rhythms of plants and also regulates physiological processes including growth, flowering time, nitrogen cycle (Covington and Harmer, 2008) and photosynthesis (Sun et al., 2003). In different periods of light, plants can respond to the diurnal cycle by changing the growth potential ratio, or by different growth rates of roots, stems, and leaves. For example, in the early stage of light exposure, maize circadian rhythm can prepare for plant to increase light by up regulating photosynthesis related genes (Khan et al., 2010). Plant aquaporin proteins gene is also regulated by time rhythm. For example, the aquaporin proteins of rice root changes with time rhythm (Sakurai et al., 2008). The circadian rhythm of leaf movement was affected in transgenic plants with impaired expression of plasma membrane aquaporin gene NtAOP1 (Siefritz et al., 2004). Aquaporin protein PIPs are involved in the radial water movement of vascular bundle sheath cells and mesophyll cells in C₄ plant maize. However, it has not been reported that PIPs and C₄ cycle related genes are jointly regulated by the time rhythm.

There are 11 members of the PIP subfamily of maize aquaporin protein. So far, few studies have investigated the relationship between the specific expression of aquaporin proteins in vascular bundle sheath cells and C₄ photosynthesis. In this study, through the combination of bioinformatics and gene expression analysis, a gene named ZmPIP4c was determined among the 11 members of the PIP subfamily contained in maize, which was highly specifically expressed in vascular bundle sheath cells, indicating that it should play an important role in the water transport and storage of C₄ maize vascular bundle sheath cells. Therefore, we analyzed the expression of ZmPIP4c gene under the conditions of leaf development gradient, circadian rhythm, salt stress, etc., in order to have a deeper understanding of the C₄ cycle mediated by maize bundle sheath cell specific aquaporin protein.

1 Results and Analysis

1.1 Domain analysis of the ZmPIP4c protein

ZmPIP4c protein was analyzed using MOTIF-search online software (Figure 1), and the results showed that the only domain of ZmPIP4c was MIP. The domains were amino acids from the 46^th to the 275^th positions. The MIP domain can facilitate the passive transport of small molecules and promote the bidirectional transport of water molecules on the cell membrane.

1.2 Analysis of physicochemical properties, hydrophilicity and hydrophobicity, and subcellular localization of ZmPIP4c protein

Analyzed the physicochemical properties of ZmPIP4c protein, it could be found that the molecular weight of ZmPIP4c protein was 30724.58 Da, pI was 8.3, instability coefficient was 35.95. It belongs to basic amino acid and stable protein. In addition, the hydrophilicity and hydrophobicity analysis of the protein showed that the hydrophobicity ratio of ZmPIP4c protein was 63.93%, and ZmPIP4c protein was predicted to be hydrophobic. Besides, ZmPIP4c protein contains 6 transmembrane helical, indicating that it is a typical transmembrane protein.

The subcellular localization of ZmPIP4c protein was predicted, and the probability of its localization on the cell membrane was more than 60%. Therefore, its localization was predicted on the cell membrane.

1.3 Prediction of secondary structure and tertiary structure of ZmPIP4c protein

PROFsec secondary structure analysis software was used to predict the ZmPIP4c protein, and it was found that the proportion of α-helix in ZmPIP4c protein was the highest, accounting for more than 45%. Therefore, the secondary structure of ZmPIP4c protein is mainly composed of α-helix.

3DLigandSite was used to predict the tertiary structure of ZmAMT5c protein, and it was found that ZmAMT5c protein was mainly composed of α-helix, accounting for 59% (Figure 2). Therefore, both the secondary and tertiary structures predicted that the protein was mainly composed α-helix.

1.4 Expression analysis of ZmPIP4c gene and C₄ photosynthesis related gene

The leaf gradient expression data of ZmPIP4c gene and C₄ photosynthesis gene were retrieved from maize genome database (Figure 3). In leaves, the expressions of ZmPIP4c gene and C4 cycling related gene NAD-malic enzyme gene (NAD-ME), phosphoenolpyruvate carboxylase gene (PEPC) and carbonic anhydrase gene (CA). The expressions of these genes all showed gradual increase from leaf base to leaf tip, and reached the highest level at the tip (Figure 3A). Then the expression values of ZmPIP4c gene, NAD-ME, PEPC and CA in time rhythm were collected from the database (Figure 3B). The expression of ZmPIP4c gene increased gradually from midnight to noon, peaked at noon, and then decreased to dusk. Data of ZmPIP4c gene, NAD-ME, PEPC and CA under abiotic salt stress were obtained from Genevestigator (Figure 3C). All genes were down regulated under salt stress. Then, we used Maize eFP to detect the specific expression of ZmPIP4c gene, NAD-ME, PEPC and CA genes in maize leaf cells. The results showed that ZmPIP4c and NAD-ME genes were highly expressed in vascular bundle sheath cells, while PEPC and CA were highly expressed in mesophyll cells (Figure 4).

2 Discussion

After a series of bioinformatics analysis, we predicted that the aquaporin protein ZmPIP4c is a typical transmembrane protein with 6 transmembrane helices. The physicochemical properties of ZmPIP4c protein were analyzed and it was found that ZmPIP4c protein was a stable protein with hydrophobicity. The secondary structure and tertiary structure analysis showed that the protein was mainly α-helix.

NAD-ME, PEPC and CA are all genes closely related to the C₄ cycle. NAD-ME catalyzes the decarboxylation of malic acid to release CO₂ and produce pyruvic acid, which makes the C₄ pathway to circulate. PEPC catalyzes the formation of oxaloacetic acid from PEP and CO₂ in C₄ pathway. In C₄ plants, CA can catalyze the mutual transformation between CO₂ and HCO₃^-, and provide inorganic carbon source for phosphoenolpyruvate carboxylase (Momayyezi et al., 2020). All expressions of NAD-ME, PEPC, CA, and ZmPIP4c genes showed gradual increase from leaf base to leaf tip, and reached the highest level at the tip (Figure 3A). It is known that the photosynthetic intensity of leaves increases gradually from the base to the tip (Pick et al., 2011), indicating that the expression patterns of these four genes are positively correlated in different parts of leaves. In addition, previous studies showed that with the enhancement of photosynthesis, leaves also had an increased demand for transport of small molecules such as water and CO₂ (Field et al., 1991), and the aquaporin protein gene could not only transport water in plants, but also transport small molecules such as CO₂ (Chaumont et al., 2001). It could be seen that the expression of ZmPIP4c gene increased along the leaf gradient, which could assist the photosynthetic function part of the leaves to carry out photosynthesis smoothly. What's more, as the marker gene of C₄ photosynthesis, the expression pattern of C₄ specific expression genes such as NAD-ME can be used to screen transcription genes with similar expression pattern, while transcription genes with similar expression pattern will play a role in the same or related pathway (Pick et al., 2011). The results showed that aquaporin protein gene ZmPIP4c (Figure 3A; Figure 4), which had the same expression pattern as NAD-ME, was closely related to C₄ cycle in maize leaves. Therefore, ZmPIP4c could be used as a candidate gene to further study the not yet indicated new C₄ characteristics of C₄ plants such as maize.

In contrast, the most significant structural difference between C₄ plants and C₃ plants is that C₄ plants have expanded vascular sheath cells and chloroplasts. The specific expressions of ZmPIP4c, NAD-ME, PEPC, and CA genes in maize leaf cells were analyzed, and it was found that ZmPIP4c and NAD-ME were highly specifically expressed in vascular bundle sheath cells, while PEPC and CA were highly specifically expressed in mesophyll cells (Figure 4). The results showed that ZmPIP4c and NAD-ME played an important role in C₄ maize vascular sheath cells, while PEPC and CA played an important role in C₄ maize mesophyll cells. ZmPIP4c in leaves is highly specifically expressed in vascular bundle sheath cell, facilitating more water to be stored in sheath cells, so as to balance water supply of mesophyll cells and maintain normal physiological metabolism of plants (Liu et al., 2013). On the other hand, the expanded bundle sheath cells of C₄ maize could store a large amount of water through the specific high expression of aquaporin protein gene in vascular sheath cells, which could prevent the damage of leaves caused by excessive transpiration in hot climate (Liu et al., 2013). Indeed, there is a coupling mechanism between water transport and transpiration in plant tissues, which is crucial for plant productivity. For example, aquaporin protein can regulate stomatal opening and transpiration by buffering water potential, and promote carbon fixation and growth of plants (Maurel et al., 2016). It is well known that C₄ plants have higher water use efficiency than C₃ plants, but the related molecular mechanisms are still poorly understood. The high expression of ZmPIP4c in the vascular bundle sheath once again indicates that this gene is involved in the composition of the cell-specific characteristics of C₄ leaves.

The circadian cycle enables plants to develop self-sustaining rhythms under light conditions, and at the same time regulates photosynthesis (Maurel et al., 2008). Plants also adapt to changes in photosynthesis by regulating gene expression and protein activity (Irvine, 1971). Sun et al. (2003) found that many photosynthesis related genes, such as NAD-ME, are affected by the circadian cycle, and show regular changes in plants. It was showed the expression of ZMPIP4C gene, NAD-ME, PEPC, and CA in 6 different periods of circadian circulation (Figure 3B). And can be seen that the expression of ZMPIP4C gene and the other three genes increased and reached the peak from midnight to noon. From noon to dusk, the expression of ZmPIP4c and three other genes decreased gradually. The expression trend of ZmPIP4c gene was consistent with that of C₄ photosynthesis related genes in circadian rhythm. Caldeira et al. (2014) found that the transpiration water of plants is up to 200% of their water content every day. In order to avoid water waste and enable plants to grow normally, their water status changes greatly from night to day. Circadian rhythms in maize lead to changes in transpiration demand and affect photosynthesis, which is related to the rapid changes of plant photosynthetic hydraulic conduction, especially the expression of PIP aquaporin proteins (Caldeira et al., 2014). From midnight to noon, plants respond to low-intensity light in the morning detected by internal photoreceptors. The increase of transpiration increases water use efficiency and the expression of aquaporin (Nada and Abogadallah, 2014). At the same time, low intensity light activated photosynthesis (Dodd et al., 2015). Zmpip4c was expressed at the beginning of light to transport water for genes related to photosynthesis of bundle sheath cells and provide the required liquid phase environmental matrix to maintain plant water status (Maurel et al., 2016). Photosynthesis was activated and CA gene responded to the increased photosynthetic expression (Momayyezi et al., 2020), which provided bicarbonate for PEPC to form the precursor molecule of C₄ acid under the action of PEPC, and played a role in the primary fixation of carbon (Studer et al., 2014). In order to prepare the proteins required for photosynthesis, the expression of NAD-ME and other related genes increased (Hayes et al., 2010), and the increased expression of NAD-ME converted the C₄ intermediate into the C₃ intermediate pyruvic acid, accelerating the C₄ reaction in the bundle sheath (Dodd et al., 2015). From noon to dusk, the expression of ZmPIP4c and other three genes decreased gradually. It was found that the expression of aquaporin protein in leaves is positively correlated with transpiration (Vandeleur et al., 2009; POU et al., 2013). The decrease of light intensity led to the decrease of transpiration efficiency and the expression of aquaporin protein. And a rapid decrease in plant water balance due to the shortage of leaf water supply, stomatal closure, and decreased photosynthesis (Nada and Abogadallah, 2014). The decrease of transpiration resulted in the decrease of ZmPIP4c expression, the decrease of water supply of sheath cell leaves and the decrease of photosynthetic rate. NAD-ME, PEPC, and CA genes all transited to post photosynthetic state, and their expression gradually decreased (Dodd et al., 2015). In conclusion, the specific expression of aquaporin protein ZmPIP4c in bundle sheath cells and its expression trend in time rhythm are consistent with the expression trend of C₄ photosynthesis gene, which effectively controls the water transport required by photosynthesis of bundle sheath cells under transpiration, provides sufficient water environment for the efficient operation of C₄ photosynthesis, and avoids water waste.

Salt stress is a common abiotic stress in plant growth. In maize leaves, the expression of ZmPIP4c gene was down-regulated under salt stress (Figure 3C), while NAD-ME, PEPC and CA in maize leaves were down-regulated under the same experimental conditions. It has been shown that photosynthetic rate in C₄ maize leaves decreased under salt stress (Hichem et al., 2009). Salt stress caused plant cells to establish osmotic potential to prevent roots from absorbing water, stomatal closure, limiting CO₂ entry into leaves, resulting in decreased photosynthesis (Moshelion et al., 2014), leading to down regulation of C₄ cycle genes such as NAD-ME and PEPC. Meanwhile, CA gene is an essential substance for photosynthesis, providing bicarbonate for photosynthesis, and its activity is affected by photosynthetic rate (Studer et al., 2014). Therefore, CA gene expression also shows a downward trend. The decrease of photosynthetic rate led to the increase of stomatal resistance and the decrease of leaf water conductivity, which led to the decrease of ZmPIP4c expression in leaves. In addition, BS cells are closely connected with mesophyll cells through plasmodesma. Vascular bundle sheath cells and mesophyll cells also have close hydraulic connection and feedforward regulation (Sade et al., 2014). Studies have shown that aquaporin protein in bundle sheath cells can directly control the water in bundle sheath cells and indirectly control the water conduction in mesophyll cells. After silencing the aquaporin protein in bundle sheath cells, the water conductivity in mesophyll cells decreased (Sade et al., 2014). The expression of aquaporin protein ZmPIP4c in the bundle sheath decreased under salt stress, and the expression of CA and PEPC specifically expressed in mesophyll cells decreased, which may be due to the decrease of water conductivity of mesophyll cells and the failure of CA to transform CO₂ normally, which resulted in the down regulation of PEPC and NAD-ME in mesophyll. This provided additional evidence to support the existence of BS-ME blade hydraulic conduction signals. In conclusion, the expression trend of this aquaporin protein is the same as that of the key C₄ gene under salt stress, proving once again that this aquaporin protein is closely related to the C₄ cycle.

In conclusion, a series of bioinformatics analysis and gene expression analysis showed that ZmPIP4c was not only a hyd-rophobic with MIP domain, but its expression trend in leaf gradient was the same as that of C4 photosynthesis related gene. ZmPIP4c was highly expressed in vascular bundle sheath cells and participated in the formation of cell-specific characteristics of C₄ leaves, indicating that ZmPIP4c was C₄ specific component, closely related to C₄ cycle. ZmPIP4c is not only consistent with the expression trend of C₄ photosynthesis related genes NAD-ME, PEPC and CA in circadian rhythm, but also provides sufficient water environment for the efficient operation of C₄ photosynthesis and avoids water waste. It also responds to salt stress together with NAD-ME, PEPC and CA, which provides additional evidence for the existence of hydraulic conduction signal in BS-ME leaves. And this will help us to understand the molecular mechanism of cell-specific aquaporin protein genes involved in the C₄ cycle.

3 Materials and Methods

3.1 Data sources

Maize aquaporin protein coding sequence was obtained by searching the NCBI website (Table 1), which was named ZmPIP4c according to the subfamily and the location of this protein on the chromosome.

3.2 Domain analysis of aquaporin protein

MOTIF-search (Table 1) was used to draw the domain of ZmPIP4c protein, and then analyzed its conservative and functional domains.

3.3 Analysis of ZmPIP4c protein physical and chemical properties, hydrophilicity and hydrophobicity, and sub celluar location

Protparam program of ExPASy website (Table 1) was used to analyze the basic physical and chemical properties of maize ZmPIP4c protein. ProtScale online software (Table 1) was used to analyze and predict the maize ZmPIP4c protein hydrophilicity and hydrophobicity. And PSORT (Table 1) was used to predict the ZmPIP4c protein sub celluar location.

3.4 Secondary structure and tertiary structure prediction of ZmPIP4c protein

PROFsec (Table 1) was used to analyze the secondary structure of ZmPIP4c protein sequence. The ZmPIP4c protein sequence was then submitted to the RaptorX server to predict the tertiary structure (Källberg et al., 2012).

3.5 Expression analysis of ZmPIP4c gene and cell specific expression analysis of related photosynthetic genes

The specific expression of the aquaporin protein gene was analyzed in vascular bundle sheath cells and mesophyll cells with the help of Maize eFP Browser. The leaf gradient gene expression RNA-seq data were retrieved from maize genome database, and the gene chip expression values of maize leaves under biological stress and abiotic stress were retrieved from Genevestigator database, and then mapped by software HemI1.0.

Authors’ contributions

LX designed and carried out this experiment, performed the statistical analysis and drafted the manuscript. LYL participated in the design of the experiment and performed the statistical analysis. LZ conceived of the study, and guide its design, data analysis, draft of the manuscript. MZY guide the revision of the manuscript. All authors read and approved the final manuscript.

Acknowledgments

This study was supported by the Special Project for Introduction of Talent of Hebei Agricultural University (YJ2020003).

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