Research Article

Identification and Bioinformatics Analysis of ABC Transporter Gene Family in Hydrangea under Aluminum Stress  

Haixia Chen , Xuan Wang , Lu Xu
Horticulture College of Hunan Agricultural University, Hunan Mid-subtropical Quality Plant Breeding and Utilization Engineering Technology Research Center, Changsha, 410128, China
Author    Correspondence author
Molecular Plant Breeding, 2022, Vol. 13, No. 31   doi: 10.5376/mpb.2022.13.0031
Received: 15 Dec., 2022    Accepted: 22 Dec., 2022    Published: 30 Dec., 2022
© 2022 BioPublisher Publishing Platform
This article was first published in Molecular Plant Breeding in Chinese, and here was authorized to translate and publish the paper in English under the terms of Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Preferred citation for this article:

Chen H.X., Wang X., and Xu L., 2022, Identification and bioinformatics analysis of ABC transporter gene family in hydrangea under aluminum stress, Molecular Plant Breeding, 13(31): 1-15 (doi: 10.5376/mpb.2022.13.0031)

Abstract

ABC transporters is a type of transmembrane transporters widely found in prokaryotes and eukaryotes. They are involved in plant signal transduction, secondary metabolite transport and abiotic stress response. According to the transcriptome data of Hydrangea, this study was proposed analyze the members of ABC transporter gene family, physical and chemical properties, gene structure, phylogeny and gene expression patterns under aluminum stress using bioinformatics method. The results showed that there were 48 members of ABC transporter gene family in Hydrangea, which belonged to 7 subfamilies respectively, among which the C subfamily had the most members; the subcellular localization results showed that 50% of the family members were located on the plasma membrane; the physical and chemical properties and domain analysis showed that most of the ABC transporters were hydrophobic proteins, and different subfamilies had specific conserved motifs, but motif1 and motif2 were all present in hydrangea ABC transporter; A phylogenetic tree was constructed with 129 ABC transporters of Arabidopsis thaliana, and 48 ABC transporters from Hydrangea were clustered into 7 subfamilies of Arabidopsis thaliana respectively. The expression profile analysis showed that the HmABCA1, HmABCC1, HmABCC6, HmABCC14 and HmABCD1 gene were upregulated in the root and HmABCG1 gene were up-regulated in leaves after aluminum stress treatment. The results provide a reference for further study on aluminum tolerance and expression regulation of ABC transporter genes in hydrangea.

Keywords
Hydrangea macrophylla; Aluminum tolerance; ABC transporter genes; Bioinformatics

ABC transporters (ATP-binding cassette transporters) is a type of transmembrane transporters widely found in prokaryotes and eukaryotes, which could transport substrates, including sugar, amino acids, proteins, metal ions and other biological molecules, across the membrane with the help of the energy generated by ATP hydrolysis. They are involved in a variety of biological processes, such as plant hormone transport, signal transduction, cell detoxification, virus defense and antigen transmission (Wilkens, 2015; Aryal et al., 2016). ABC transporter family has a conservative structure. The typical structure is composed of two nucleotide binding domains (NBD) and two transmembrane domains (TMD). NBD domain is relatively conservative, which performs ATP hydrolase function and provides energy for transmembrane transport. TMD is a transmembrane channel, and its structure and sequence have substrate specificity (Lane et al., 2016).

 

In the early 1990s, the first ABC transporter AtABCB1 was first found in Arabidopsis thaliana, and then ABC transporters were identified from more than 20 plants such as rice (Oryza sativa), tobacco (Nicotiana tabacum) and maize (Zea mays). At the same time, the mechanisms of ABC transporters' transmembrane transport, absorption and transport of nutrient ions, and resistance to abiotic stress were studied. ABC transporters can improve the resistance of crops to abiotic stresses such as high temperature, drought, salinity and heavy metals. ABC transporters could improve the resistance of crops to abiotic stresses such as high temperature, drought, salinity and heavy metals. Studies have shown that the ABCB transporter AtABCB27/AtTAP2, located in the vacuolar membrane and vascular system of Arabidopsis root tips, transports aluminum into vacuoles in the form of chelating peptide conjugates to isolate, thereby improving plant aluminum tolerance (Larsen et al., 2007). OsSTAR1 and OsSTAR2 identified from indica rice are ABC transporter genes in response to aluminum stress, which transport UDP-glucose to limit aluminum accumulation and reduce aluminum toxicity. Another semi-molecular transporter OsALS1 is in vacuolar membrane and encodes aluminum transporter (Huang et al., 2012). Subsequently, homologous genes were identified in maize (Zea mays), sweet sorghum (Sorghum bicolor), alfalfa (Medicago sativa) and other plants, all of which belong to ABC transporters related to aluminum toxicity stress (Song et al., 2013; Liang, 2018).

 

Hydrangea is an aluminum enriched plant. Aluminum treatment for a few months can make the accumulation of aluminum in leaves reach 5 mg/g dry weight, and the aluminum content in leaf cells is 15.7 mmol/kg fresh weight. These aluminums are absorbed by roots and transported to plants to chelate with citric acid in a molar ratio of 1:1 to synthesize a non-toxic citric acid aluminum complex. Therefore, it is considered that there should be a system for aluminum ion absorption, transport and storage in hydrangea. In order to clarify the correlation between blue hydrangea coloration and aluminum ion transport, two aluminum ion transporter genes HmPALT1 and HmVALT located on the plasma membrane and vacuolar membrane respectively were isolated and identified from the blue hydrangea sepals, both of which belong to the anion permease family (Negishi et al., 2012). The amino acid permeability enzyme family gene HmPALT2 cloned from blue sepals is located in the plasma membrane and expressed in all tissues of plants. It participates in the transportation of many ions and can also transport aluminum ions from extracellular to cytosol (Negishi et al., 2013). Therefore, the molecular mechanism of response to aluminum stress and enrichment in hydrangea plants has always been a research hotspot. Transcriptome sequencing analysis showed that the genes encoding ABC transporters were up-regulated in roots and leaves of Hydrangea after aluminum stress, but no systematic study of ABC transporter gene family was carried out, and its gene function was unclear (Chen et al., 2015). According to the transcriptome data of Hydrangea, ABC transporters were selected as keywords in the gene function annotation library in this study, and the obtained ABC transporters were identified, and bioinformatics analyzed to explore the relationship between ABC transporter family and aluminum resistance, in order to provide a theoretical basis for the function mining of ABC transporter gene family.

 

1 Results and Analysis

1.1 Identification and physical and chemical properties analysis of ABC transporter in hydrangea

The 95 714 gene clusters in the transcriptome of hydrangea were searched in the three databases of GO, NR and KEGG with ABC transporters as the keywords. A total of 208 gene clusters were annotated, which belong to seven ABC transporter subfamilies, namely ABCA, ABCB, ABCC, ABCD, ABCE, ABCF and ABCG. SMART was used to predict the domain of 208 ABC transporters, and the conserved NBDs domain was selected as the final screening index. A total of 48 ABC transporters in hydrangea with NBDs domain were screened (Table 1).

 


Table 1 The ABC transporter protein family members and physico-chemical analysis in Hydrangea

 

The online software ProtParam was used to predict the physical and chemical properties of the protein encoded by the ABC transporter gene family in hydrangea (Table 1). The length of 48 ABC transporters in hydrangea is ranged from 195 to 1 895 aa, and the theoretical value of molecular weight is 21413.55~104980.71. The theoretical isoelectric point (pI) is 5.18~9.49, of which 28 are acidic proteins with pI less than 7 and the remaining 20 are basic proteins. Instability coefficient analysis showed that 38 proteins are stable proteins with instability coefficient less than 40, and the remaining 10 are unstable proteins. The aliphatic index is 80.4~111.16, with an average value of 96.33, of which 19 have an aliphatic index higher than 100. A relatively high aliphatic index could maintain good stability of protein and help to play a normal function in different environments. The grand average of hydropathicity is -0.625~0.287, of which 30 are negative, indicating that most of them are hydrophobic proteins, and the hydrophobic degree is different.

 

Based on the subcellular localization analysis of ABC transporter gene family in hydrangea, it was found that it was distributed in plasma membrane, chloroplast, mitochondria, cytoplasm and nucleus. The three ABCA subfamily genes were located on the plasma membrane; Three ABCB subfamily genes were located in plasma membrane, mitochondria and chloroplast, respectively; Most of the 17 ABCC subfamily genes were located in the plasma membrane, and only one was located in the mitochondria; Only one of the ABCD subfamily genes was located in the plasma membrane and the other six were located in the chloroplast; The four genes of ABCE subfamily were located in plasma membrane, cytoplasm, chloroplast and nucleus, respectively; 13 ABCF subfamily genes were distributed in plasma membrane, cytoplasm, chloroplast and nucleus; One ABCG subfamily gene was located in the plasma membrane. Therefore, 50% of the ABC transporter genes of hydrangea are located in the plasma membrane, and 94.1% of the ABCC subfamily genes are located in the plasma membrane, which is common with the known plant ABC transporters, indicating that the ABC transporter family has a certain degree of conservation in function and plays a role in transmembrane material transport and information transmission.

 

1.2 Phylogenetic analysis of ABC transporters in Hydrangea

According to the sequence similarity as the classification basis of gene subfamilies, the phylogenetic tree was constructed by using ClustalW software for the 48 ABC transporter sequences in Hydrangea (Figure 1). The members of the ABC transporter family in Hydrangea could be divided into 7 subfamilies, of which the ABCC subfamily contained up to 17 protein members, followed by the ABCF subfamily with 13 protein members. ABCC subfamily proteins are all molecule ABC transporters, which are involved in many physiological processes in plants, including maintaining intracellular balance, metal detoxification and transporting glutathione conjugates (Wilkens, 2015). 17 and 15 ABCC transporter members have been identified in rice and Arabidopsis genomes, respectively. Therefore, it is speculated that the ABCC transporter in Hydrangea under aluminum stress may participate in the transmembrane transport of aluminum ions. The ABCB and ABCC transporter subfamilies in Hydrangea are in the same branch, and it is speculated that the two subfamily genes have homology. The proteins in the ABCF subfamily belong to soluble ABC proteins, with two nucleic acid domains and no transmembrane domain. It was found that the ABCF3 gene in Arabidopsis thaliana plays an important role in the response to cadmium stress (Li, 2018). Therefore, it is speculated that the ABCF subfamily genes in Hydrangea may also be involved in the process of responding to aluminum stress.

 


Figure 1 Evolution tree of ABC transporter in Hydrangea

 

In order to further study the evolutionary relationship of the members of the ABC transporter family in Hydrangea, a phylogenetic tree was constructed by using the 129 ABC protein sequences published in Arabidopsis and 48 protein sequences in Hydrangea (Figure 2). Referring to the Sanchez-Fernandez et al. (2001), 129 ABC transporters in Arabidopsis were classified into 7 subfamilies, and the 48 ABC transporters in Hydrangea were also clustered into 7 subfamilies with the help of PLA (Proximity Ligation Assay). Therefore, according to the position of phylogenetic tree, the function of ABC transporter in Hydrangea could be preliminarily identified.

 


Figure 2 Phylogenetic tree of ABC transporter proteins from Hydrangea and Arabidopsis thaliana

Note: Shade blue: ABC transporters in Hydrangea

 

1.3 Analysis of ABC transporter domains and conserved motifs in Hydrangea

CD-search was used to analyze the ABC protein domains of Hydrangea, and it was shown that each protein has one or two highly conserved nucleotide domains, and some subfamilies contain several transmembrane domains (Figure 3; Table 1). There are 24 ABC transporters with two nucleotide domains, of which 14 belong to the ABCC subfamily, because the C subfamily has only one type of whole molecule protein. ABCE subfamily and ABCF subfamily proteins do not have transmembrane domains and do not function as transporters, but participate in ribosome biosynthesis and translation regulation.

 


Figure 3 Domain distribution of ABC transporter family in Hydrangea

 

MEME online software was used to predict the conserved motifs of 48 ABC transporters in Hydrangea, and it was found that the number of conserved motifs of different proteins was different, and the types were different (Figure 4). There were 50 motif conserved motifs in the ABC transporters of Hydrangea, of which motif1 and motif2 existed in all ABC transporters. Motif3 and motif13 appeared 28 times and motif4 appeared 27 times, all of which were distributed in each subfamily. ABCB and ABCC subfamilies shared motifs of motif5~12, 16, 19, 23, 25, 27, 29, 30, 36, 39, 41, 44, 47, 49, 50, so it was speculated that the two subfamilies have homology. Motif18, 20, 31, 33, 35, 37, 40, 42, 45, 46, 48 were distributed in the ABCF subfamily. Motif21, 28, 34, 38 were distributed in the ABCD subfamily. Motif22, 24, 26, 32, 43 were distributed in the ABCE subfamily. Conserved motifs clustered in the same subfamily are similar in composition, indicating that the evolutionary relationship between members is close. There are differences in conserved motifs among different subfamilies. The higher the frequency of motif, the higher the degree of conservation.

 


Figure 4 Distribution of conserved motifs of ABC transporter family in Hydrangea

Note: Different color squares represent different conservative motifs

 

1.4 Analysis of differential expression pattern

In order to analyze the expression pattern of ABC transporter gene, the transcriptome data of roots and leaves in Hydrangea under aluminum stress for 4 h were screened and the expression results of 48 ABC transporter genes were analyzed, with the no aluminum stress treatment as control. The heat map of the expression patterns of 48 ABC transporter genes in the roots and leaves was drawn with the help of pheatmap software (Figure 5). The results showed that all transporter genes were expressed in the roots of Hydrangea, but 38 genes were slightly expressed or not expressed in the leaves. Compared with the Hydrangea without aluminum stress treatment, 12 genes were up-regulated in the root and only 1 gene was up-regulated in the leaf after aluminum stress. Among them, there were 6 genes with significant differences in expression (Table 2), which were HmABCA1, HmABCC1, HmABCC6, HmABCC14 and HmABCD1 expressed in the root and HmABCG1 expressed in the leaf. Therefore, it is believed that the ABC transporter gene in the root of Hydrangea is involved in the absorption, transport and storage of aluminum ions in response to aluminum stress.

 


Figure 5 The heat map of ABC transporter gene expression under Al stress in Hydrangea

Note: T1: -Al treatment in root; T2: -Al treatment in leaf; T3: +Al treatment in root; T4: +Al treatment in leaf

 


Table 2 Differential expression of ABC transporter gene in hydrangea under aluminum stress

 

2 Discussion

This study systematically analyzed the response of 48 ABC transporter genes in Hydrangea to aluminum stress. The results showed that the expression of different genes was different in the root and leaf after aluminum stress treatment, and the root was the main part of Hydrangea in response to aluminum stress. Based on the phylogenetic tree analysis, 48 proteins were clustered into 7 subfamilies, and the clustering results were basically consistent with the ABC transporters of Arabidopsis, indicating that the ABC transporters in Hydrangea and Arabidopsis have high homology, which provides a reference for the functional analysis of the ABC transporters of Hydrangea.

 

Through the analysis of the evolutionary relationship of the ABC transporter family between Hydrangea and Arabidopsis, it was found that HmABCA3 (c211005.graph_c0) and Arabidopsis AtABCA1/AtAOH1 (AT2G41700) clustered in one branch; HmABCA2 (c210858.graph_c0) was closely related to AtABCA9/AtATH15, which encoded an ABC transporter located in the endoplasmic reticulum (Kim et al., 2013; Wang et al., 2017). There are few studies on the function of subfamily A transporters in plants. According to homology analysis, they have the function of lipid transport in plants.

 

Subfamily B proteins in plants have diverse functions and are mainly involved in the transport of auxin, secondary metabolites and heterologous substances, including multidrug resistance related protein (MDR), ABC transporter of the mitochondria (ATM), heavy metal tolerance protein (HMT) and transporter associated with antigen processing (TAP). ABCB27/AtTAP2 (AT5G39040), which is located in the same branch as HmABCB1 (c162347.graph_c1) of Hydrangea, encodes an ABCB transporter located in the vacuole. The gene product may play an important role in the intracellular transport of aluminum chelates and is an important factor in the aluminum sequestration mechanism (Larsen et al., 2007). After aluminum stress, HmABCB1 in Hydrangea was up-regulated in the root, but the differential expression was not significant, which may be related to the concentration and time of aluminum stress treatment.

 

The original member of subfamily C was the human multidrug resistance related protein HsMRP1, and MRPs were subsequently found in plants. MRP is not only involved in intracellular detoxification and oxidative stress resistance, but also mediates the transport of glutathione (GSH) conjugates. ABC transporters on the vacuolar membrane are mainly members of PRP subfamily, which are mainly involved in the transport of toxic substances and realize their isolation by vacuoles, thus playing a detoxification role. HmABCC4HmABCC5HmABCC12 (c176480.graph_c0, c185684.graph_c0, c210623.graph_c0) in Hydrangea and ABCC8/ATMRP6ABCC10/ATMRP14 (AT3G59140.1, AT3G21250.1) in Arabidopsis are clustered in the same branch. At present, it has been reported that ATMRP14 is a heterologous transmembrane transporter, and ATMRP6 has an important role in detoxifying cadmium (Gaillard et al., 2008). ABCC5/AtMRP5 (AT1G04120.1), which is clustered with the HmABCC15 (c211939.graph_c0) in Hydrangea, participates in the regulation of ion channels in abscisic acid and calcium ion signal transduction pathways in guard cells, helping plants resist drought. The expression of ABCC13/AtMRP11 (AT2G07680.1), which is similar to the relationship between HmABCC8 (c201746.graph_c0) in Hydrangea, is induced by gibberellin and inhibited by naphthalene acetic acid, abscisic acid and zeatin. In the presence of cadmium or hydrogen peroxide, the differential expression of ABCC13 gene in the root system of wheat seedlings plays an important role in alleviating the oxidative stress caused by heavy metals (Bhati et al., 2015). HmABCC1 (c156671.graph_c0), HmABCC6 (c194263.graph_c0) and HmABCC14 (c211816.graph_c0) clustered into independent branches in the evolutionary tree, and their expression levels were significantly increased after aluminum stress. It is speculated that they participated in the response of Hydrangea to aluminum stress, and the mechanism of their response to aluminum stress needs further study.

 

The ABCD subfamily belongs to PMP subfamily, also known as peroxisome transmembrane transport proteins. There are only two kinds of AtPMP1 and AtPMP2 in Arabidopsis. The six genes in ABCD subfamily in Hydrangea are clustered in the same group with ABCD1 (AT4G39850.1). It is reported that ABCD1 is involved in the physiological process of glucose regulated meristem maintenance in Arabidopsis roots (Huang et al., 2019). In the process of aluminum stress, a series of complex oxidative stress reactions occur after the roots are damaged. Therefore, the function of HmABCD1 (c145066.graph_c1) gene, which is significantly upregulated in the roots of Hydrangea, deserves further study.

 

The ABCG subfamily is a transporter of the NBD-TMD reverse sequence domain type, including two types of PDR and WBC. It has been reported that AcABCG1 gene in Axonopus compressus is localized on the cytoplasmic membrane in response to aluminum stress (Li et al., 2019). HmABCG1 (c187439.graph_c0) in Hydrangea and AtABCG14 (AT1G31770.1) in Arabidopsis clustered on the same branch. AtABCG14 is a cytokinin transporter, which can not only regulate the growth and development of Arabidopsis root, but also mediate cytokinin transport to regulate the drought resistance response (Ko et al., 2013; Zhang et al., 2014). Therefore, it can be speculated that the root tip of Hydrangea is damaged after aluminum stress, and the expression of HmABCG1 gene is up-regulation. In response to aluminum stress, its gene function needs further study.

 

3 Materials and Methods

3.1 Identification of ABC transporter gene family members in Hydrangea

The data used to identify the members of the ABC transporter gene family in Hydrangea is the transcriptome sequencing data obtained by our research group based on the Illumina high-throughput sequencing platform (Chen et al., 2015). As there is no genomic information of the Hydrangea, according to the NR annotation results, the ABC transporters of the Hydrangea were screened by using "ATP-binding cassette transporters" or "ABC" as the keywords. Then NCBI-blastp program was used to compare the screened sequences with the ABC transporter gene families of 22 species such as Arabidopsis, papaya and grape. Then, the SMART online database was used to analyze the conserved domain of the above genes, and the sequences that did not contain the ABC transporter gene features were removed, so as to obtain the transcript sequence of the ABC transporter gene of Hydrangea. According to the ABC transporter gene naming pattern of Arabidopsis thaliana, it was named based on sequence similarity, and the unigenes in the transcriptome database were renumbered accordingly.

 

ProtParam online software (https://web.expasy.org/protparam/) was used to predict and analyze the molecular weight, isoelectric point, instability index, aliphatic index, hydrophobicity and other physical and chemical properties of the ABC transporter sequence of Hydrangea. Plant-mPloc online software (http://www.csbio.sjtu.edu.cn/bioinf/plant/) was used for subcellular localization prediction of proteins. The protein conserved motif was analyzed by MEME online software (http://meme-suite.org/tools/meme), and the ABC protein domain was predicted by CD-search, and the gene structure map was drawn.

 

3.2 Construction of the phylogenetic tree of ABC transporter gene family in Hydrangea

Selected the amino acid sequence of the identified ABC family gene of Hydrangea. mafft software was used to conduct multiple sequence alignment of ABC protein. Neighbor joining (NJ) method was used to construct evolutionary tree (MEGA7).

 

3.3 Comparative study on ABC transporter gene family members between Arabidopsis and Hydrangea

First, download the amino acid sequence of Arabidopsis thaliana from the website, and then use Muscle software for global alignment. Use iqtree software to construct the evolutionary tree, with the base substitution model of LG+F+G4. Finally, iTOL software was used to color the evolutionary tree.

 

3.4 Analysis of expression pattern

In order to construct the expression profile of ABC transporter gene in different tissues of Hydrangea under aluminum stress, analyze the tissue expression specificity of ABC transporter gene, obtain the FPKM value of the gene expressed in roots and leaves without aluminum stress treatment and 4 h stress treatment from the transcriptome database, and finally draw the gene expression heat map with pheatmap software.

 

Authors’ contributions

CHX and WX are the executors of the experimental design and research of this study, completed the data analysis and wrote the first draft of the paper. WX and XL participated in the experimental design and analysis of the experimental results. CHX is the designer and principal of the project, guiding the experimental design, data analysis, writing and revision of the paper. All authors read and approved the final manuscript. 

 

Acknowledgements

This study was supported by the National Natural Science Foundation of China (31201656) and the Natural Science Foundation of Hunan Province (2017JJ3105).

 

References

Aryal B., Laurent C., and Geisler M., 2016, Correction: learning from each other: ABC transporter regulation by protein phosphorylation in plant and mammalian systems, Biochemical Society Transactions, 44(2): 663-673

https://doi.org/10.1042/BST20150128_2

PMid:27068986

 

Bhati K.K., Sharma S., Aggarwal S., Kaur M., Shukla V., Kaur J., Mantri S., and Pandey A.K., 2015, Genome-wide identification and expression characterization of ABCC-MRP transporters in hexaploid wheat, Front. Plant Sci., 6: 488

https://doi.org/10.3389/fpls.2015.00488

PMid:26191068 PMCid:PMC4486771

 

Chen H.X., Lu C.P., Jiang H., and Peng J.H., 2015, Global transcriptome analysis reveals distinct aluminum-tolerance pathways in the al-accumulating species hydrangea macrophylla and marker identification, PLoS One, 10(12): e0144927

https://doi.org/10.1371/journal.pone.0144927

PMid:26660093 PMCid:PMC4682798

 

Gaillard S., Jacquet H., Vavasseur A., Leonhardt N., and Forestier C., 2008, AtMRP6/AtABCC6, an ATP-Binding Cassette transporter gene expressed during early steps of seedling development and up-regulated by cadmium in Arabidopsis thaliana, BMC Plant Biol., 8: 22

https://doi.org/10.1186/1471-2229-8-22

PMid:18307782 PMCid:PMC2291051

 

Huang C.F., Yamaji N., Chen Z.C., and Ma J.F., 2012, A tonoplast-localized half-size ABC transporter is required for internal detoxification of aluminum in rice, Plant J., 69: 857-867

https://doi.org/10.1111/j.1365-313X.2011.04837.x

PMid:22035218

 

Huang L., Yu L.J., Zhang X., Fan B., Wang F.Z., Dai Y.S., Qi H., Xie L.J., ang Xiao S., 2019, Autophagy regulates glucose-mediated root meristem activity by modulating ROS production in Arabidopsis, Autophagy, 15(3): 407-422

https://doi.org/10.1080/15548627.2018.1520547

PMid:30208757 PMCid:PMC6351127

 

Kim S., Yamaoka Y., Ono H., Kim H., Shim D., Maeshima M., Martinoia E., Cahoon E.B., Nishida I., and Lee Y., 2013, AtABCA9 transporter supplies fatty acids for lipid synthesis to the endoplasmic reticulum, Proc. Natl. Acad. Sci. USA, 110(2): 773-778

https://doi.org/10.1073/pnas.1214159110

PMid:23269834 PMCid:PMC3545803

 

Ko D., Kang J., Kiba T., Park J., Kojima M., Do J., Kim K.Y., Kwon M., Endler A., Song W.Y., Martinoia E., Sakakibara H., and Lee Y., 2014, Arabidopsis ABCG14 is essential for the root-to-shoot translocation of cytokinin, Proc. Natl. Acad. Sci. USA, 111(19): 7150-7155

https://doi.org/10.1073/pnas.1321519111

PMid:24778257 PMCid:PMC4024864

 

Lane T.S., Rempe C.S., Davitt J., Staton M.E., Peng Y.H., Soltis D.E.,Melkonian M., Deyholos M., Leebens-Mack, H J., Chase M., Rothfels C.J., Stevenson D., Graham S.W., Yu J., Liu T., Pires J.C., Edger P.P., Zhang Y., Xie Y.L., Zhu Y., Carpenter E., Wong G.K., and Jr C.N.S., 2016, Diversity of ABC transporter genes across the plant kingdom and their potential utility in biotechnology, BMC Biotechnol., 16: 47

https://doi.org/10.1186/s12896-016-0277-6

PMid:27245738 PMCid:PMC4886425

 

Larsen P.B., Cancel J., Rounds M., and Ochoa V., 2007, Arabidopsis ALS1 encodes a root tip and stele localized half type ABC transporter required for root growth in an aluminum toxic environment, Planta, 225(6): 1447-1458

https://doi.org/10.1007/s00425-006-0452-4

PMid:17171374

 

Li J.F., Han J.R., Jia Y.D., Zhang L.Z., Wang W.Q., Wang Z.Y., and Chen Z.J., 2019, Cloning and expression analysis of AcABCG1 in Axonopus compressus, Caodi Xuebao (Acta Agrestia Sinica), 27(5): 1147-1153

 

Li S.2018. The functional study of ABCF subfamily genes in Arabidopsis thaliana. University of Chinese Academy of Sciences, Supervisor: Xu J. pp.24-34 

 

Liang Y.N., 2018, Functional analysis of SbSTAR1 and SbSTAR2 in sweet sorghum (Sorghum bicolor L.) under aluminum stress, Thesis for M.S., College of Plant Science, Jilin University, Supervisor: Yang Z.M. pp.36-45

 

Negishi T., Oshima K., Hattori M., and Yoshida K., 2013, Plasma membrane-localized Al-transporter from blue hydrangea sepals is a member of the anion permease family, Genes to Cells, 18: 341-352

https://doi.org/10.1111/gtc.12041

PMid:23433438

 

Negishi T., Oshima K., Hattori M., Kanai M., Mano S., Nishimura M., and Yoshida K., 2012, Tonoplast-and plasma membrane-localized aquaporin-family transporters in blue hydrangea sepals of aluminum hyperaccumulating plant, PloS One, 7(8): e43189

https://doi.org/10.1371/journal.pone.0043189

PMid:22952644 PMCid:PMC3430636

 

Sanchez-Fernandez R., Davies T.G.E., Coleman J.O.D., and Rea P.A., 2001, The Arabidopsis thaliana ABC protein superfamily, a complete inventory, Journal of Biological Chemistry, 276(32): 30231-30244

https://doi.org/10.1074/jbc.M103104200

PMid:11346655

 

Song W.J., Wang P.Q., Zhang B.Y., Yang Q.C., Cai B.J., Lai P., and Kang Y.H., 2013, MsSTAR2 encodes a half-type ATP-binding cassette transporter protein that is induced by aluminum in Medicago sativa L., Nongye Shengwu Jishu Xuebao (Journal of Agricultural Biotechnology), 21(5): 522-529

 

Wang X.Z., Sun W.M., Ma Y.F., Han E.Q., Han L., Sun L.P., Peng Z.H., and Wang B.J., 2017, Research progress of Arabidopsis ABC transporter, Zhiwu Shengli Xuebao (Plant Physiology Journal), 53(2): 133-144

 

Wilkens S., 2015, Structure and mechanism of ABC transporters, F1000 Prime Reports, 7(14): 14-18

https://doi.org/10.12703/P7-14

PMid:25750732 PMCid:PMC4338842

 

Zhang K.W., Novak O., Wei Z.Y., Gou M.Y., Zhang X.B., Yu Y., Yang H.J., Cai Y.H., Strnad M., and Liu C.J., 2014, Arabidopsis ABCG14 protein controls the acropetal translocation of root-synthesized cytokinins, Nat. Commun., 5: 3274

https://doi.org/10.1038/ncomms4274

PMid:24513716