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Review

ATP-Binding Cassette G Transporters and Their Multiple Roles Especially for Male Fertility in Arabidopsis, Rice and Maize

by
Suowei Wu
*,†,
Chaowei Fang
†,
Ziwen Li
,
Yanbo Wang
,
Shuangshuang Pan
,
Yuru Wu
,
Xueli An
,
Yan Long
and
Xiangyuan Wan
*
Zhongzhi International Institute of Agricultural Biosciences, Shunde Graduate School, Research Center of Biology and Agriculture, University of Science and Technology Beijing (USTB), Beijing 100024, China
*
Authors to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Int. J. Mol. Sci. 2022, 23(16), 9304; https://doi.org/10.3390/ijms23169304
Submission received: 17 July 2022 / Revised: 11 August 2022 / Accepted: 16 August 2022 / Published: 18 August 2022
(This article belongs to the Special Issue Advances and Innovations in Maize Genetics and Breeding Research)
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Abstract

:
ATP-binding cassette subfamily G (ABCG) transporters are extensive in plants and play essential roles in various processes influencing plant fitness, but the research progress varies greatly among Arabidopsis, rice and maize. In this review, we present a consolidated nomenclature and characterization of the whole 51 ABCG transporters in maize, perform a phylogenetic analysis and classification of the ABCG subfamily members in maize, and summarize the latest research advances in ABCG transporters for these three plant species. ABCG transporters are involved in diverse processes in Arabidopsis and rice, such as anther and pollen development, vegetative and female organ development, abiotic and biotic stress response, and phytohormone transport, which provide useful clues for the functional investigation of ABCG transporters in maize. Finally, we discuss the current challenges and future perspectives for the identification and mechanism analysis of substrates for plant ABCG transporters. This review provides a basic framework for functional research and the potential application of ABCG transporters in multiple plants, including maize.

1. Introduction

ATP-binding cassette (ABC) transporter, one of the largest proteins family, widely exists in bacteria, animals, and plants [1]. ABC transporters are involved in countless cellular processes, including the transmembrane transport of various unrelated molecules [2]. ABC proteins possess nucleotide-binding domain (NBD) which contain several highly conserved motifs, including the Walker A and B sequences, the ABC signature motif, the H loop and the Q loop; and transmembrane domains (TMDs), each composed of several hydrophobic α-helices [1,3]. ABC proteins can be full-size (with two TMDs and two NBDs) or half-size (with one TMD and one NBD), in which case they may function as homodimer or heterodimer [2]. The two NBDs cooperate to bind and hydrolyze ATP, providing the energy for transport, and the TMDs are involved in substrate recognition and translocation across the lipid bilayer [3]. In plants, ABC proteins can be divided into eight subfamilies, including ABCA to ABCG, and ABCI. Among them, the ABCG subfamily is the largest one in plants, and there are 43 and 54 members in Arabidopsis and rice, respectively [3]. The outstanding diversification of ABCGs is thought to be associated with plant adaptation to land environment [4]. In Arabidopsis and rice, ABCG transporters have been widely studied and linked with anther and pollen development, cuticle formation, defense response, hormone transport, and seed germination [2]. The substrates of ABCG transporters, including lipids, hormones, and heavy metal ions, etc., have been unambiguously identified using isotope labeling experiments in vivo, or indirectly by imprecise measurements using the GC-MS system [5]. However, the actual substrates of most ABCG transporters remain uncharacterized.
It has been reported that 54 ABCG members exist in maize [6], but only three ABCG transporters (ZmMS2/ZmABCG26, ZmMS13 and ZmGL13) have been characterized and reported to be required for male fertility or leaf cuticle formation in maize [7,8,9,10]. Notably, the current nomenclature of the maize ABCG subfamily does not comply with the standard naming system used in Arabidopsis and rice [3,6], and thus results in a lot of inconveniences and problems in maize ABCG research.
Here, we present a consolidated nomenclature system for the maize ABCG subfamily, and focus on functional research progress of the reported ABCG genes in Arabidopsis and rice, and their implications for maize orthologs. The functions of maize ABCG genes can be predicted by homologous and bioinformatic analyses. Furthermore, we summarize the current progress and challenges in the identification of ABCG substrates, and present the future research directions and potential applications for ABCG proteins in plants.

2. The ABCG Transporters in Maize and Their Phylogenetic Analysis

2.1. The Nomenclature and Characterization of the Maize ABCG Subfamily

A consolidated nomenclature for maize ABCG transporters will provide much needed clarity and a framework for future research. Based on BLAST searches against the maize B73 reference genome (B73 RGV4.0) in the MaizeGDB database (https://maizegdb.org/ (accessed on 8 May 2022)), a total of 51 ABCG genes were identified in maize, and named as ZmABCG1 to ZmABCG51 according to their domain organizations (including 31 half-size ABCGs with one NBD-TMD and 20 full-size ABCGs with two NBD-TMD) and chromosome locations in maize (Table 1). Among them, 34 ZmABCGs have synonyms in MaizeGDB, including different members with the same name, such as two members (Zm00001d028689 and Zm00001d013960) named ABCG2, four members (Zm00001d032601, Zm00001d002871, Zm00001d048621 and Zm00001d020811) named ABCG11, etc., which will lead to confusion in the functional research of maize ABCG transporters in the future. Thus, it is desirable to create a unified nomenclature before the confusing and repeated ABCG names proliferate further.
Notably, the total number (51) of maize ABCG genes is different from that (54) in the previous report [6], which may have resulted from an alternative splicing of three ABCG genes, including ZmABCG5, ZmABCG7 and ZmABCG12 (Table S1). Furthermore, the spatial expression patterns of maize ABCG genes, based on RNA-seq data analyses in MaizeGDB, are shown in Table 1. These will provide useful information for investigating their biological functions. Other characteristics of the 51 ZmABCG genes, including the corresponding gene models in B73 reference genome (B73v3), genome physical locus, topology, and subcellular localization prediction using Cell-PLoc 2.0 (http://www.csbio.sjtu.edu.cn/bioinf/Cell-PLoc-2/ (accessed on 20 April 2022)), are listed in Table S1. All of the 51 ZmABCG genes are distributed across the 10 chromosomes of maize, varying in numbers from eight on chromosome 8, to two on chromosome 5 (Table 1, Figure 1). The chromosome location information of ABCGs will be helpful in exploring their function and evolution in the future.

2.2. Phylogenetic Analysis and Classification of ABCGs

In order to analyze the evolutionary relationship of ABCGs in maize, rice and Arabidopsis, the maximum likelihood method and the MEGA7 program were used to construct the phylogenetic tree, based on the multiple alignment of all the ABCG protein sequences in these tree plant species. All the identified ABCGs were divided into two subgroups in the phylogenetic tree (Figure 2). Subgroup 1 contains 90 half-size ABCGs, including 31 in maize, 31 in rice and 28 in Arabidopsis, which can be further classified into five clades (Clades 1-1 to 1-5). Among them, some ABCGs have been reported to be involved in anther and pollen development, such as AtABCG9 [11], AtABCG26 [12,13,14], OsABCG15 [15,16] and ZmABCG27 (ZmMS2) [8,10] in Clade 1-1, AtABCG11 [17], OsABCG26 [18,19], ZmABCG13 (ZmMS13) [7] in Clade 1-2, AtABCG1/16 [20,21,22], and OsABCG3 [23,24] in Clade 1-4. Notably, the ABCGs in Clade 1-4 can be classified into two subclades of monocots and dicots, indicating that diversification of these ABCG members is later than that between monocots and dicots during plant evolution. Subgroup 2 consists of 58 full-size ABCGs, including 20 in maize, 23 in rice and 15 in Arabidopsis, which can be further classified into three clades (Clades 2-1 to 2-3). Considering that some of the ABCGs have been functionally characterized in Arabidopsis and rice and several maize orthologs of Arabidopsis and rice, known ABCGs have been reported to play similar roles during anther development and male fertility, such as the orthologous ZmABCG27 (previously named as ZmMS2/ZmABCG26) [8,10], OsABCG15 [15,16] and AtABCG26 [12,13,14], the orthologous ZmABCG13 (previously named as ZmMS13) [7], OsABCG26 [18,19] and AtABCG11 [17]. Therefore, the phylogenetic analysis result will provide helpful information in exploring the functions of unknown ABCG genes in maize.

3. Multiple Functions of ABCG Transporters in Arabidopsis, Rice and Maize

To date, at least 30 ABCG genes in Arabidopsis and 11 ABCG genes in rice have been functionally characterized, but only three ABCG genes have been identified in maize. These reported ABCG transporters play essential roles in various biological processes, such as anther and pollen development, vegetive and female organ development, biotic and abiotic stress response, and phytohormone transport and signaling (Table 2; Figure 3).

3.1. Anther and Pollen Development

ABCG transporters are involved in the translocation of various cuticular wax and cutin monomers, sporopollenin precursors, and tryphine components, from the tapetum where they are generated, to the anther outer surface and locule for anther cuticle and pollen wall formation, respectively (Figure 3A). Loss-function mutations of some ABCG transporters often lead to defective anther cuticle and pollen wall formation and thus lead to male sterility in plants.
To date, at least 12 ABCG genes have been reported to be required for anther/pollen development and male fertility in multiple plant species (Table 2). For example, Arabidopsis AtABCG11 acts as both homodimer or heterodimer with other ABCGs (e.g., AtABCG5, 9, 12 and 14), and plays multiple roles in flower cuticle formation, root suberin metabolism, and proper vascular development. The abcg11 mutant displays dwarfism, male sterility, post-genital organ fusions, and reduced cutin load in flowers [17,25,26]. OsABCG26 and ZmMS13, orthologs of AtABCG11 in rice and maize, are essential for anther cuticle and pollen exine formation, especially for the translocation of the cuticular wax and cutin monomers generated in the tapetum across anther wall layers for anther cuticle formation [7,18,19]. AtABCG26 and its orthologs OsABCG15 in rice and ZmMS2 in maize, play similar roles in controlling pollen exine development and male fertility by mainly transferring sporopollenin precursors from the tapetum onto the developing microspore surface, although loss-of-function mutations of OsABCG15 and ZmMs2 also lead to defective anther cuticle formation [8,10,15,16]. Arabidopsis AtABCG1 and AtABCG16, and their rice ortholog OsABCG3, are required for the transport of nexine and intine precursors for male gametophyte development in the post-meiotic stages, and for pollen tube growth; the atabcg1atabcg16 double mutant and osabcg3 mutant show defective nexine and intine formation, and thus male fertility [21,22,23,24]. Furthermore, AtABCG9 and AtABCG31 are involved in the specific transport of steryl glycosides from the tapetum for pollen coat (tryphine) deposition [11]. Most recently, Liu et al. has reported that AP1/2β adaptins mediated exocytosis of tapetum-specific ABCG transporters (such as AtABCG9 and AtABCG16) from the trans-Golgi network (TGN) to the plasma membrane, and are required for pollen development in Arabidopsis [70]. AtABCG28 is specifically expressed in mature pollen grains and pollen tubes, and is critical for localizing polyamines [precursors of reactive oxygen species (ROS)] at the growing pollen tube tip in Arabidopsis [31]. Together, ABCG transporters may play conserved and divergent roles in transferring various precursors essential for anther development and male fertility in monocots (rice and maize) and dicots (Arabidopsis).

3.2. Vegetative and Female Organ Development

Additionally, several ABCG transporters are reported to be involved in the formation of diffusion barriers, such as cuticle, suberin, and lignin, during the vegetative and female organ development in plants (Table 2, Figure 3B). For example, AtABCG5, a half-size transporter of cutin and wax precursors, is required for the dense cuticle layer formation in young seedlings, forming homodimer or heterodimers with AtABCG11, and possibly with AtABCG12 and other ABCG transporters [33]. AtABCG11, but not AtABCG12, forms a homodimer to transport wax and cutin precursors, and AtABCG11 forms a heterodimer with AtABCG12 to transport wax precursors from the cuticle layer in Arabidopsis [26]. AtABCG13 is required for the secretion of flower cuticular lipids, particularly in petals and carpels [37], similar to the full-size AtABCG32 transporter, which exports particular cutin precursors from the epidermal cell in leaves and flowers [43]. AtABCG27 and AtABCG33 may be involved in cellulose synthesis, based on expression analysis using Arabidopsis cell suspensions during tracheary element differentiation [40]. Furthermore, the orthologs of Arabidopsis AtABCG32, rice OsABCG31 [45] and maize ZmGL13 [9] are also essential for leaf cutin and cuticular wax formation. Notably, four half-size Arabidopsis ABCG transporters, AtABCG1, AtABCG2, AtABCG6, and AtABCG20 [21,27], as well as their rice ortholog OsABCG5/RCN1 [34] are responsible for the transport of suberin monomers in roots and seed coats, and OsABCG5/RCN1 is also essential for shoot branching, by promoting the outgrowth of lateral shoots [35]. AtABCG29 acts as a monolignol (p-coumaryl alcohol) transporter involved in lignin biosynthesis [42]. Collectively, ABCG transporters play indispensable roles in the formation of various diffusion barriers in plants, which are critical for plant growth and the development against various stresses.

3.3. Biotic and Abiotic Stress Response

Another important function of ABCG transporters is in the protection against biotic and abiotic stresses (Table 2, Figure 3C). Many ABCG transporters are involved in pathogen and other biotic stress responses by the secretion of defense molecules. For example, AtABCG34 mediated the secretion of camalexin to defend against the necrotrophic pathogens Alternaria brassicicola and Botrytis cinerea [47], and AtABCG36/PEN3 was reported to enhance resistance against several non-adapted pathogens [58]. AtABCG36/PEN3 and AtABCG40/PDR12 mediate camalexin secretion for the resistance against Botrytis cinerea [63]. The half-size ABC transporters STR1 and STR2 are indispensable for mycorrhizal arbuscule formation in rice [64]. Increasing reports reveal that ABCG transporters perform important physiological functions in plant drought stress response by regulating stomatal closure, such as OsABCG5/RCN1 [50], AtABCG17 and AtABCG18 [67], AtABCG21 and AtABCG22 [39,68], AtABCG25 [69], and AtABCG40 [62], while OsABCG9 plays a critical role in the transportation of epicuticular wax and is essential for rice drought response [53]. Overexpression of the AtABCG19 transporter confers kanamycin resistance to transgenic plants, which may be related to zinc homeostasis in plants [51,52]. Furthermore, AtABCG35, AtABCG36 and their rice ortholog OsABCG36, as well as OsABCG43, are involved in cadmium tolerance and other heavy metal stresses [54,55,56,60]. Together, ABCG transporters play critical roles in various biotic and abiotic stress responses in plants by transporting different substrates.

3.4. Hormone Transport and Signaling

In addition, ABCG transporters are also involved in phytohormone transport, which is very important for plant growth and development, including seed germination, shoot development, root formation, stress response, and other physiological processes [71]. To date, at least four types of hormones transported by 14 transporters have been identified in Arabidopsis and rice (Table 2, Figure 3D). Among them, Arabidopsis AtABCG14 is essential for the long-distance translocation of cytokinins from root to shoot [65], and its ortholog, OsABCG18, plays a similar role in rice and promotes grain yield [66]. Several ABCGs have been identified as ABA transporters that are required for the long-distance translocation of ABA in Arabidopsis and rice, such as AtABCG17 and AtABCG18 [67], AtABCG22 [68], AtABCG25 [69], AtABCG30, AtABCG31, and AtABCG40 [30,62], and OsABCG5 [50]. While auxin and its precursors (IBA) are reported to be transported by ABCG transporters, including AtABCG1 and AtABCG16 [20], AtABCG36 [59], and AtABCG37 [49], the ABCG transporters AtABCG1 and AtABCG16 are also involved in subcellular distribution in the metabolism and signaling of Jasmonates [29].
In summary, some ABCG transporters play different roles during plant growth and development, as they may function as homodimers and/or heterodimers with different ABCGs and thus transport various substrates.

4. Functional Predictions of ABCG Genes in Maize

Compared with Arabidopsis and rice, less ABCG genes have been functionally identified in maize (Table 2). Considering the functional conservation of orthologs during plant evolution, maize ABCG genes might also play similar roles with their orthologs, as with Arabidopsis and rice. Moreover, the spatiotemporal expression patterns of genes are often associated with their biological functions. Therefore, homologous and bioinformatics analyses will provide useful information for exploring the function of maize ABCG genes.

4.1. Functional Prediction of ABCGs Based on Homologous Analysis

Multiple studies have shown that some ABCG orthologs of Arabidopsis, rice, and maize play both conserved and divergent roles in regulating anther development and male fertility. For example, ZmABCG27/ZmMS2 and its orthologs OsABCG15 and AtABCG26, are all required for the translocation of sporopollenin lipidic precursors from the tapetum to the locules for pollen exine development in maize, rice, and Arabidopsis [8,10,13,14,15,19]. ZmABCG13/ZmMS13 is essential for anther cuticle and pollen exine formation, consistent with its orthologs AtABCG11 and OsABCG26 in Arabidopsis and rice [7,17,19]. Here, we list the maize orthologs of all identified ABCG genes in Arabidopsis and rice (Table 2), which will provide an important clue for the functional characterization of maize ABCG genes by reverse genetic strategies, such as CRISPR/Cas9 or RNAi. For example, given that AtABCG9 and AtABCG31 are essential for the deposition of steryl glycosides on the pollen coat, and thus for pollen fitness [11], and OsABCG3 and its orthologs AtABCG1/16 are required for pollen wall (nexine and intine layers) formation [18,21,22,24], their orthologs in maize might also be involved in pollen wall development, which needs to be confirmed in the future via reverse genetic strategies. Therefore, it is feasible to predict the functions of more unknown ABCG genes in maize using homologous analysis.

4.2. Functional Prediction of ABCGs Based on Bioinformatic Analysis

The expression analysis based on RNA sequencing (RNA-seq) data provides a new window to predict gene function. Based on anther RNA-seq data, there are 62 putative maize genic male-sterility (GMS) genes, 125 putative lipid metabolic GMS genes, and 112 putative sugar metabolic GMS genes which have been predicted in maize [72,73,74]. Additionally, some of these predicted GMS genes have been verified through CRISPR/Cas9 mutagenesis in maize [8,75]. Thus, bioinformatic analysis, such as RNA-seq data analysis, provides an effective way to predict the functions of unknown genes.
Here, we carried out transcriptomic analyses of all maize ABCG members based on the RNA-seq data from four maize inbred lines W23, B73, Oh43, and Zheng58 developing anthers (Figure 4A). Based on the RNA-seq data analyses, the 51 maize ABCG genes can be classified into two clusters (I and II). Cluster I can be further divided into four subclusters: I-1 to I-4. Subcluster I-1 consists of six ABCG genes, and half of them (ZmABCG22, ZmABCG8 and ZmABCG24) show peak expressions at middle anther stages (S8 to S9–10), and half of them (ZmABCG10, ZmABCG11 and ZmABCG34) display peak expressions at late anther stages (S11 or S12), in agreement with the qPCR results (Figure 4B1–B6). Interestingly, the rice ortholog (OsABCG3) of ZmABCG8 and ZmABCG24, and Arabidopsis ortholog (AtABCG31) of ZmABCG34 have been reported as being required for pollen wall development and male fertility [11,21], indicating that these ABCGs are most likely involved in anther and pollen development in maize. Subcluster I-2 and I-3 include eight and 26 ABCG members, respectively, with relatively low expression during different anther developmental stages. Notably, ZmABCG26 and ZmABCG14 in subcluster 1–3, show an anther-specific expression pattern based on the RNA-seq data retrieved from the MaizeGDB website (http://www.maizegdb.org/ (accessed on 20 April 2022)), and they are orthologs of AtABCG28 required for pollen tube growth and male fertility in Arabidopsis [28], indicating that ZmABCG26 and ZmABCG14 might also be required for pollen tube growth in maize. This needs to be proven by reverse genetics. Subcluster I-4 includes three ABCG genes with multiple expression peaks in developing anthers (Figure 4B7–B9), including ZmABCG2 which is orthologous to AtABCG1/16 [21,22], suggesting its potential roles in pollen wall development. Cluster II covers eight ABCG genes with relatively high expression during anther development [7,8,10] (Figure 4B10–B15), including four orthologs of the known GMS genes in Arabidopsis and rice, such as ZmABCG27/ZmMS2 orthologous to AtABCG26 and OsABCG15 [8,10,13,14,15,19], ZmABCG13/ZmMS13, ZmABCG3 and ZmABCG6 orthologous to AtABCG11 and OsABCG26 [7,17,19], and two of them (ZmABCG27 and ZmABCG13), but not ZmABCG3, have been confirmed to be required for male fertility in maize [7,8,10], implying that these orthologous ABCG genes play both conserved and diversified roles during anther development among different plants.

5. Substrate Identification of Plant ABCG Transporters

Although ABCG transporters take part in various physiological processes in plants, the exact substrates of most ABCG transporters are still unclear. The functional insights into plant ABCG transporters are mainly gained from reverse genetics (e.g., CRISPR/Cas9 mutagenesis) and metabolite analysis. However, the phenotypic effects resulting from knockout studies might be pleiotropic, thus hindering the identification of the actual substrates.
The most powerful approach to identify the substrates of ABCG transporters is to use a transport assay which demonstrates translocation activity across a membrane in a strictly ATP-dependent manner. The prerequisite for the transport assay is the overexpression of the ABCG protein in a proper expression system, such as tobacco (N. benthamiana) protoplast system and yeast strains (YMM12 and BY-2) cell lines [30,44,49]. To date, substrates of ten Arabidopsis ABCG transporters have been identified by employing radioactivity labeled compounds, i.e., by using isotope labeling experiments in vivo (Table 3). For example, Arabidopsis AtABCG11 and AtABCG32 are reported to export cutin precursors (e.g.,10,16-diOH, C16:0-2-glycerol and W-OH C16:0) for plant cuticle formation, based on the export assay using the protoplast system of N. benthamiana [44]. Four AtABCG transporters collaboratively deliver ABA from the endosperm to the embryo for controlling seed germination: AtABCG25 and AtABCG31 export ABA from the endosperm, whereas AtABCG30 and AtABCG40 import ABA into the embryo [30]. However, many isotope labeling compounds are not commercially available and these experiments are time consuming, which hinders their extensive utilization and efficiency.
An alternative approach is the substrate analysis of ABCG mutant and wild-type plant tissues using the GC-MS system. Here, a rational guess about the substrate or substrate class can be made by using the metabolite analysis of specific plant tissues, such as anthers, roots and leaves. The substrates of at least 15 ABCG transporters in Arabidopsis, rice and maize have been predicted based on this approach (Table 3). One advantage of this approach is that mixtures, such as the content of the plant’s cytosol, can be directly employed, and subsequently, the isolated compounds can be used as direct proof. Thus, this is a very powerful approach in identifying the substrate of ABCG transporters, although the conclusion is not very convincing. For example, ZmMS13 and ZmMS2 encoding ZmABCG13 and ZmABCG27, respectively, are reported to be essential for the transport of anther cuticle and sporopollenin precursors, partly due to the lipidomic analysis of the wild-type and mutant mature anthers, using GC-MS [7,10].
Besides the two approaches mentioned above, other direct or indirect transport assays have also been reported to have been used to identify the substrates of ABCG transporters. For example, the lipidic substrates of AtABCG1 and ZmMS13/ZmABCG13 were indicated by the ATPase assay of purified protein in vitro [7,27], Cytokinin was identified as the substrate of OsABCG18 based on an export assay with a heterologous expression of OsABCG18 in the protoplast system of N. benthamiana [66], and AtABCG28 was required for the apical accumulation of reactive oxygen species in growing pollen tubes based on the immunostaining of polyamines in the growing tip of pollen tubes [31] (Table 3).
Notably, although the substrate identification of plant ABCG transporters has gained some encouraging progress, the translocated substrates and the detailed transport mechanisms of the majority of ABCG proteins remain unclear, which need to be investigated in the future.

6. Conclusions and Perspective

ABCG transporters, as one of the largest subfamilies of ABC transporters, play critical roles in various processes influencing plant fitness, especially in plant reproductive and vegetative organ development, hormone transport and stress response. Compared with the unified named ABCG transporters in Arabidopsis and rice [3], the ABCG transporters in maize lack a standard naming system, leading to confusion in the functional research of maize ABCGs. In this review, we firstly established a consolidated nomenclature and chromosome location map of the 51 ABCG transporters in the maize genome (Table 1 and Figure 1), providing a basic framework for future research. Based on the phylogenetic analysis, the whole ABCG subfamily members in Arabidopsis, rice and maize can be divided into two subgroups and eight clades (Figure 2). These results will provide useful clues for exploring the functions of unknown ABCG genes in maize. Secondly, we summarized the latest research progress of ABCG transporters present in Arabidopsis, rice, and maize. The functions of the reported ABCG transporters are involved in diverse processes, such as anther and pollen development, vegetative and female organ development, abiotic and biotic stress response, and phytohormone transport (Table 2 and Figure 3). Thirdly, compared with the plentiful in-depth studies of ABCGs in Arabidopsis and rice, less ABCG transporters in maize have been functionally characterized to date. We thus provide two methods for the functional prediction of ABCG transporters in maize, namely the homologous and bioinformatic analyses, based on the functional conservation of ABCG orthologs during plant evolution and spatiotemporal expression patterns of ABCG genes in maize (Table 1 and Figure 4). Finally, we summarize and discuss the current approaches and challenges in the substrate identification of plant ABCG transporters, including the transport assays, by employing radioactivity compounds in vivo, metabolite analysis, using the GC-MS system, and other direct or indirect transport assays (Table 3), although the actual substrates of most plant ABCG transporters remain largely unknown.
In summary, given the tremendous progress in defining the critical roles of plant (mainly in Arabidopsis and rice) ABCG transporters involved in various biological processes influencing male fertility and plant fitness, it is plausible that the corresponding ABCG orthologs might also play similar roles in other crops, including maize. This can be verified by the use of reverse genetics (e.g., CRISPR/Cas9 mutagenesis analysis), and thus deepen our understanding of the functional mechanism of ABCG transporters in multiple plants. The derived mutant lines with elite characters, such as male sterility or higher fitness, have potential applications in hybrid crop breeding and seed production in the future.

Supplementary Materials

The supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/ijms23169304/s1.

Author Contributions

Conceptualization, S.W. and X.W.; methodology, C.F., Z.L. and Y.W. (Yanbo Wang); validation, C.F., S.P. and Y.W. (Yuru Wu); formal analysis, S.W. and C.F.; resources, C.F., S.P. and Y.W. (Yuru Wu); writing—original draft preparation, S.W. and C.F.; writing—review and editing, S.W., X.A., Y.L. and X.W.; funding acquisition, S.W., X.A., Y.L. and X.W. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the National Key Research and Development Program of China (2021YFF1000302, 2021YFD1200700), the National Natural Science Foundation of China (31871702, 31971958, 32172057), and the Fundamental Research Funds for the Central Universities of China (06500060).

Institutional Review Board Statement

The study did not require ethical approval.

Informed Consent Statement

Not applicable.

Data Availability Statement

All data are shown in the main manuscript and in the Supplementary Materials.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Higgins, C.F. ABC transporters: From microorganisms to man. Annu. Rev. Cell. Biol. 1992, 8, 67–113. [Google Scholar] [CrossRef] [PubMed]
  2. Lefevre, F.; Boutry, M. Towards identification of the substrates of ATP-binding cassette transporters. Plant Physiol. 2018, 178, 18–39. [Google Scholar] [CrossRef] [PubMed]
  3. Verrier, P.J.; Bird, D.; Burla, B.; Dassa, E.; Forestier, C.; Geisler, M.; Klein, M.; Kolukisaoglu, U.; Lee, Y.; Martinoia, E.; et al. Plant ABC proteins-a unified nomenclature and updated inventory. Trends Plant Sci. 2008, 13, 151–159. [Google Scholar] [CrossRef]
  4. Hwang, J.U.; Song, W.Y.; Hong, D.; Ko, D.; Yamaoka, Y.; Jang, S.; Yim, S.; Lee, E.; Khare, D.; Kim, K.; et al. Plant ABC transporters enable many unique aspects of a terrestrial plant’s lifestyle. Mol. Plant 2016, 9, 338–355. [Google Scholar] [CrossRef] [PubMed]
  5. Do, T.H.T.; Martinoia, E.; Lee, Y.; Hwang, J.U. 2021 update on ATP-binding cassette (ABC) transporters: How they meet the needs of plants. Plant Physiol. 2021, 187, 1876–1892. [Google Scholar] [CrossRef]
  6. Pang, K.; Li, Y.; Liu, M.; Meng, Z.; Yu, Y. Inventory and general analysis of the ATP-binding cassette (ABC) gene superfamily in maize (Zea mays L.). Gene 2013, 526, 411–428. [Google Scholar] [CrossRef]
  7. Fang, C.; Wu, S.; Niu, C.; Hou, Q.; An, X.; Wei, X.; Zhao, L.; Jiang, Y.; Liu, X.; Wan, X. Triphasic regulation of ZmMs13 encoding an ABCG transporter is sequentially required for callose dissolution, pollen exine and anther cuticle formation in maize. J. Adv. Res. 2022, 38, JARE-S-22-01434. [Google Scholar]
  8. Jiang, Y.; Li, Z.; Liu, X.; Zhu, T.; Xie, K.; Hou, Q.; Yan, T.; Niu, C.; Zhang, S.; Yang, M.; et al. ZmFAR1 and ZmABCG26 regulated by microRNA are essential for lipid metabolism in maize anther. Int. J. Mol. Sci. 2021, 22, 7916. [Google Scholar] [CrossRef]
  9. Li, L.; Li, D.; Liu, S.; Ma, X.; Dietrich, C.R.; Hu, H.C.; Zhang, G.; Liu, Z.; Zheng, J.; Wang, G.; et al. The maize glossy13 gene, cloned via BSR-Seq and Seq-walking encodes a putative ABC transporter required for the normal accumulation of epicuticular waxes. PLoS ONE 2013, 8, e82333. [Google Scholar] [CrossRef]
  10. Xu, Q.; Yang, L.; Kang, D.; Ren, Z.; Liu, Y. Maize MS2 encodes an ATP-binding cassette transporter that is essential for anther development. Crop J. 2021, 9, 1301–1308. [Google Scholar] [CrossRef]
  11. Choi, H.; Ohyama, K.; Kim, Y.Y.; Jin, J.Y.; Lee, S.B.; Yamaoka, Y.; Muranaka, T.; Suh, M.C.; Fujioka, S.; Lee, Y. The role of Arabidopsis ABCG9 and ABCG31 ATP binding cassette transporters in pollen fitness and the deposition of steryl glycosides on the pollen coat. Plant Cell 2014, 26, 310–324. [Google Scholar] [CrossRef] [PubMed]
  12. Choi, H.; Jin, J.-Y.; Choi, S.; Hwang, J.-U.; Kim, Y.-Y.; Suh, M.C.; Lee, Y. An ABCG/WBC-type ABC transporter is essential for transport of sporopollenin precursors for exine formation in developing pollen. Plant J. 2011, 65, 181–193. [Google Scholar] [CrossRef] [PubMed]
  13. Quilichini, T.D.; Friedmann, M.C.; Samuels, A.L.; Douglas, C.J. ATP-binding cassette transporter G26 is required for male fertility and pollen exine formation in arabidopsis. Plant Physiol. 2010, 154, 678–690. [Google Scholar] [CrossRef] [PubMed]
  14. Quilichini, T.D.; Samuels, A.L.; Douglas, C.J. ABCG26-mediated polyketide trafficking and hydroxycinnamoyl spermidines contribute to pollen wall exine formation in Arabidopsis. Plant Cell 2014, 26, 4483–4498. [Google Scholar] [CrossRef]
  15. Niu, B.X.; He, F.R.; He, M.; Ren, D.; Chen, L.T.; Liu, Y.G. The ATP-binding cassette transporter OsABCG15 is required for anther development and pollen fertility in rice. J. Integr. Plant Biol. 2013, 55, 710–720. [Google Scholar] [CrossRef]
  16. Qin, P.; Tu, B.; Wang, Y.; Deng, L.; Quilichini, T.D.; Li, T.; Wang, H.; Ma, B.; Li, S. ABCG15 encodes an ABC transporter protein, and is essential for post-meiotic anther and pollen exine development in rice. Plant Cell Physiol. 2013, 54, 138–154. [Google Scholar] [CrossRef]
  17. Panikashvili, D.; Shi, J.X.; Bocobza, S.; Franke, R.B.; Schreiber, L.; Aharoni, A. The Arabidopsis DSO/ABCG11 transporter affects cutin metabolism in reproductive organs and suberin in roots. Mol. Plant 2010, 3, 563–575. [Google Scholar] [CrossRef]
  18. Chang, Z.; Chen, Z.; Yan, W.; Xie, G.; Lu, J.; Wang, N.; Lu, Q.; Yao, N.; Yang, G.; Xia, J.; et al. An ABC transporter, OsABCG26, is required for anther cuticle and pollen exine formation and pollen-pistil interactions in rice. Plant Sci. 2016, 253, 21–30. [Google Scholar] [CrossRef]
  19. Zhao, G.; Shi, J.; Liang, W.; Xue, F.; Luo, Q.; Zhu, L.; Qu, G.; Chen, M.; Schreiber, L.; Zhang, D. Two ATP binding cassette g transporters, rice ATP binding cassette G26 and ATP binding cassette G15, collaboratively regulate rice male reproduction. Plant Physiol. 2015, 169, 2064–2079. [Google Scholar] [CrossRef]
  20. Liu, L.; Zhao, L.; Chen, P.; Cai, H.; Hou, Z.; Jin, X.; Aslam, M.; Chai, M.; Lai, L.; He, Q.; et al. ATP binding cassette transporters ABCG1 and ABCG16 affect reproductive development via auxin signalling in Arabidopsis. Plant J. 2020, 102, 1172–1186. [Google Scholar] [CrossRef]
  21. Yadav, V.; Molina, I.; Ranathunge, K.; Castillo, I.Q.; Rothstein, S.J.; Reed, J.W. ABCG transporters are required for suberin and pollen wall extracellular barriers in Arabidopsis. Plant Cell 2014, 26, 3569–3588. [Google Scholar] [CrossRef] [PubMed]
  22. Yim, S.; Khare, D.; Kang, J.; Hwang, J.U.; Liang, W.; Martinoia, E.; Zhang, D.; Kang, B.; Lee, Y. Postmeiotic development of pollen surface layers requires two Arabidopsis ABC-type transporters. Plant Cell Rep. 2016, 35, 1863–1873. [Google Scholar] [CrossRef]
  23. Chang, Z.; Jin, M.; Yan, W.; Chen, H.; Qiu, S.; Fu, S.; Xia, J.; Liu, Y.; Chen, Z.; Wu, J.; et al. The ATP-binding cassette (ABC) transporter OsABCG3 is essential for pollen development in rice. Rice 2018, 11, 58. [Google Scholar] [CrossRef] [PubMed]
  24. Luo, T.; Zou, T.; Yuan, G.; He, Z.; Li, W.; Tao, Y.; Liu, M.; Zhou, D.; Zhao, H.; Zhu, J.; et al. Less and shrunken pollen 1 (LSP1) encodes a member of the ABC transporter family required for pollen wall development in rice (Oryza sativa L.). Crop J. 2020, 8, 492–504. [Google Scholar] [CrossRef]
  25. Le Hir, R.; Sorin, C.; Chakraborti, D.; Moritz, T.; Schaller, H.; Tellier, F.; Robert, S.; Morin, H.; Bako, L.; Bellini, C. ABCG9, ABCG11 and ABCG14 ABC transporters are required for vascular development in Arabidopsis. Plant J. 2013, 76, 811–824. [Google Scholar] [CrossRef] [PubMed]
  26. McFarlane, H.E.; Shin, J.J.; Bird, D.A.; Samuels, A.L. Arabidopsis ABCG transporters, which are required for export of diverse cuticular lipids, dimerize in different combinations. Plant Cell 2010, 22, 3066–3075. [Google Scholar] [CrossRef]
  27. Shanmugarajah, K.; Linka, N.; Grafe, K.; Smits, S.H.J.; Weber, A.P.M.; Zeier, J.; Schmitt, L. ABCG1 contributes to suberin formation in Arabidopsis thaliana roots. Sci. Rep. 2019, 9, 11381. [Google Scholar] [CrossRef]
  28. Li, Q.; Zheng, J.; Li, S.; Huang, G.; Skilling, S.J.; Wang, L.; Li, L.; Li, M.; Yuan, L.; Liu, P. Transporter-mediated nuclear entry of jasmonoyl-isoleucine is essential for jasmonate signaling. Mol. Plant 2017, 10, 695–708. [Google Scholar] [CrossRef]
  29. Wang, F.; Yu, G.; Liu, P. Transporter-mediated subcellular distribution in the metabolism and signaling of jasmonates. Front. Plant Sci. 2019, 10, 390. [Google Scholar] [CrossRef]
  30. Kang, J.; Yim, S.; Choi, H.; Kim, A.; Lee, K.P.; Lopez-Molina, L.; Martinoia, E.; Lee, Y. Abscisic acid transporters cooperate to control seed germination. Nat. Commun. 2015, 6, 8113. [Google Scholar] [CrossRef]
  31. Do, T.H.T.; Choi, H.; Palmgren, M.; Martinoia, E.; Hwang, J.U.; Lee, Y. Arabidopsis ABCG28 is required for the apical accumulation of reactive oxygen species in growing pollen tubes. Proc. Natl. Acad. Sci. USA 2019, 116, 12540–12549. [Google Scholar] [CrossRef] [PubMed]
  32. Fedi, F.; O’Neill, C.M.; Menard, G.; Trick, M.; Dechirico, S.; Corbineau, F.; Bailly, C.; Eastmond, P.J.; Penfield, S. Awake1, an ABC-type transporter, reveals an essential role for suberin in the control of seed dormancy. Plant Physiol. 2017, 174, 276–283. [Google Scholar] [CrossRef] [PubMed]
  33. Lee, E.J.; Kim, K.Y.; Zhang, J.; Yamaoka, Y.; Gao, P.; Kim, H.; Hwang, J.U.; Suh, M.C.; Kang, B.; Lee, Y. Arabidopsis seedling establishment under waterlogging requires ABCG5-mediated formation of a dense cuticle layer. New Phytol. 2021, 229, 156–172. [Google Scholar] [CrossRef] [PubMed]
  34. Shiono, K.; Ando, M.; Nishiuchi, S.; Takahashi, H.; Watanabe, K.; Nakamura, M.; Matsuo, Y.; Yasuno, N.; Yamanouchi, U.; Fujimoto, M.; et al. RCN1/OsABCG5, an ATP-binding cassette (ABC) transporter, is required for hypodermal suberization of roots in rice (Oryza sativa). Plant J. 2014, 80, 40–51. [Google Scholar] [CrossRef]
  35. Yasuno, N.; Takamure, I.; Kidou, S.I.; Tokuji, Y.; Ureshi, A.N.; Funabiki, A.; Ashikaga, K.; Yamanouchi, U.; Yano, M.; Kato, K. Rice shoot branching requires an ATP-binding cassette subfamily G protein. New Phytol. 2009, 182, 91–101. [Google Scholar] [CrossRef]
  36. Pighin, J.A.; Zheng, H.; Balakshin, L.J.; Goodman, I.P.; Western, T.L.; Jetter, R.; Kunst, L.; Samuels, A.L. Plant cuticular lipid export requires an ABC transporter. Science 2004, 306, 702–704. [Google Scholar] [CrossRef]
  37. Panikashvili, D.; Shi, J.X.; Schreiber, L.; Aharoni, A. The Arabidopsis ABCG13 transporter is required for flower cuticle secretion and patterning of the petal epidermis. New Phytol. 2011, 190, 113–124. [Google Scholar] [CrossRef]
  38. Takeda, S.; Iwasaki, A.; Tatematsu, K.; Okada, K. The half-size ABC transporter FOLDED PETALS 2/ABCG13 is involved in petal elongation through narrow spaces in Arabidopsis thaliana floral buds. Plants 2014, 3, 348–358. [Google Scholar] [CrossRef]
  39. Kuromori, T.; Sugimoto, E.; Ohiraki, H.; Yamaguchi-Shinozaki, K.; Shinozaki, K. Functional relationship of AtABCG21 and AtABCG 22 in stomatal regulation. Sci. Rep. 2017, 7, 12501. [Google Scholar] [CrossRef]
  40. Takeuchi, M.; Kegasa, T.; Watanabe, A.; Tamura, M.; Tsutsumi, Y. Expression analysis of transporter genes for screening candidate monolignol transporters using Arabidopsis thaliana cell suspensions during tracheary element differentiation. J. Plant Res. 2018, 131, 297–305. [Google Scholar] [CrossRef]
  41. Kim, K.; Choi, B.Y.; Kang, J.; Shim, D.; Martinoia, E.; Lee, Y. Arabidopsis ABCG27 plays an essential role in flower and leaf development by modulating abscisic acid content. Physiol. Plant 2022, 174, e13734. [Google Scholar] [CrossRef] [PubMed]
  42. Alejandro, S.; Lee, Y.; Tohge, T.; Sudre, D.; Osorio, S.; Park, J.; Bovet, L.; Lee, Y.; Geldner, N.; Fernie, A.R.; et al. AtABCG29 is a monolignol transporter involved in lignin biosynthesis. Curr. Biol. 2012, 22, 1207–1212. [Google Scholar] [CrossRef] [PubMed]
  43. Bessire, M.; Borel, S.; Fabre, G.; Carraca, L.; Efremova, N.; Yephremov, A.; Cao, Y.; Jetter, R.; Jacquat, A.C.; Metraux, J.P.; et al. A member of the pleiotropic drug resistance family of ATP binding cassette transporters is required for the formation of a functional cuticle in Arabidopsis. Plant Cell 2011, 23, 1958–1970. [Google Scholar] [CrossRef] [PubMed]
  44. Elejalde-Palmett, C.; Martinez San Segundo, I.; Garroum, I.; Charrier, L.; De Bellis, D.; Mucciolo, A.; Guerault, A.; Liu, J.; Zeisler-Diehl, V.; Aharoni, A.; et al. ABCG transporters export cutin precursors for the formation of the plant cuticle. Curr. Biol. 2021, 31, 2111–2123.e9. [Google Scholar] [CrossRef]
  45. Garroum, I.; Bidzinski, P.; Daraspe, J.; Mucciolo, A.; Humbel, B.M.; Morel, J.B.; Nawrath, C. Cuticular defects in Oryza sativa ATP-binding cassette transporter G31 mutant plants cause dwarfism, elevated defense responses and pathogen resistance. Plant Cell Physiol. 2016, 57, 1179–1188. [Google Scholar] [CrossRef]
  46. Kaneda, M.; Schuetz, M.; Lin, B.S.; Chanis, C.; Hamberger, B.; Western, T.L.; Ehlting, J.; Samuels, A.L. ABC transporters coordinately expressed during lignification of Arabidopsis stems include a set of ABCBs associated with auxin transport. J. Exp. Bot. 2011, 62, 2063–2077. [Google Scholar] [CrossRef]
  47. Khare, D.; Choi, H.; Huh, S.U.; Bassin, B.; Kim, J.; Martinoia, E.; Sohn, K.H.; Paek, K.H.; Lee, Y. Arabidopsis ABCG34 contributes to defense against necrotrophic pathogens by mediating the secretion of camalexin. Proc. Natl. Acad. Sci. USA 2017, 114, E5712–E5720. [Google Scholar] [CrossRef]
  48. Fourcroy, P.; Siso-Terraza, P.; Sudre, D.; Saviron, M.; Reyt, G.; Gaymard, F.; Abadia, A.; Abadia, J.; Alvarez-Fernandez, A.; Briat, J.F. Involvement of the ABCG37 transporter in secretion of scopoletin and derivatives by Arabidopsis roots in response to iron deficiency. New Phytol. 2014, 201, 155–167. [Google Scholar] [CrossRef]
  49. Ruzicka, K.; Strader, L.C.; Bailly, A.; Yang, H.; Blakeslee, J.; Langowski, L.; Nejedla, E.; Fujita, H.; Itoh, H.; Syono, K.; et al. Arabidopsis PIS1 encodes the ABCG37 transporter of auxinic compounds including the auxin precursor indole-3-butyric acid. Proc. Natl. Acad. Sci. USA 2010, 107, 10749–10753. [Google Scholar] [CrossRef]
  50. Matsuda, S.; Takano, S.; Sato, M.; Furukawa, K.; Nagasawa, H.; Yoshikawa, S.; Kasuga, J.; Tokuji, Y.; Yazaki, K.; Nakazono, M.; et al. Rice stomatal closure requires guard cell plasma membrane ATP-binding cassette transporter RCN1/OsABCG5. Mol. Plant 2016, 9, 417–427. [Google Scholar] [CrossRef]
  51. Mentewab, A.; Matheson, K.; Adebiyi, M.; Robinson, S.; Elston, B. RNA-seq analysis of the effect of kanamycin and the ABC transporter AtWBC19 on Arabidopsis thaliana seedlings reveals changes in metal content. PLoS ONE 2014, 9, e109310. [Google Scholar] [CrossRef] [PubMed]
  52. Mentewab, A.; Stewart, C.N., Jr. Overexpression of an Arabidopsis thaliana ABC transporter confers kanamycin resistance to transgenic plants. Nat. Biotechnol. 2005, 23, 1177–1180. [Google Scholar] [CrossRef] [PubMed]
  53. Nguyen, V.N.T.; Lee, S.B.; Suh, M.C.; An, G.; Jung, K.-H. OsABCG9 is an important abc transporter of cuticular wax deposition in rice. Front. Plant Sci. 2018, 9, 960. [Google Scholar] [CrossRef] [PubMed]
  54. Oda, K.; Otani, M.; Uraguchi, S.; Akihiro, T.; Fujiwara, T. Rice ABCG43 is cd inducible and confers cd tolerance on yeast. Biosci. Biotechnol. Biochem. 2011, 75, 1211–1213. [Google Scholar] [CrossRef] [PubMed]
  55. Badri, D.V.; Loyola-Vargas, V.M.; Broeckling, C.D.; De-la-Pena, C.; Jasinski, M.; Santelia, D.; Martinoia, E.; Sumner, L.W.; Banta, L.M.; Stermitz, F.; et al. Altered profile of secondary metabolites in the root exudates of Arabidopsis ATP-binding cassette transporter mutants. Plant Physiol. 2008, 146, 762–771. [Google Scholar] [CrossRef]
  56. Kim, D.Y.; Bovet, L.; Maeshima, M.; Martinoia, E.; Lee, Y. The ABC transporter AtPDR8 is a cadmium extrusion pump conferring heavy metal resistance. Plant J. 2007, 50, 207–218. [Google Scholar] [CrossRef] [PubMed]
  57. Kim, D.Y.; Jin, J.Y.; Alejandro, S.; Martinoia, E.; Lee, Y. Overexpression of AtABCG36 improves drought and salt stress resistance in Arabidopsis. Physiol. Plant. 2010, 139, 170–180. [Google Scholar] [CrossRef] [PubMed]
  58. Stein, M.; Dittgen, J.; Sanchez-Rodriguez, C.; Hou, B.H.; Molina, A.; Schulze-Lefert, P.; Lipka, V.; Somerville, S. Arabidopsis PEN3/PDR8, an ATP binding cassette transporter, contributes to nonhost resistance to inappropriate pathogens that enter by direct penetration. Plant Cell 2006, 18, 731–746. [Google Scholar] [CrossRef]
  59. Strader, L.C.; Bartel, B. The Arabidopsis PLEIOTROPIC DRUG RESISTANCE8/ABCG36 ATP binding cassette transporter modulates sensitivity to the auxin precursor indole-3-butyric acid. Plant Cell 2009, 21, 1992–2007. [Google Scholar] [CrossRef] [PubMed]
  60. Fu, S.; Lu, Y.; Zhang, X.; Yang, G.; Chao, D.; Wang, Z.; Shi, M.; Chen, J.; Chao, D.Y.; Li, R.; et al. The ABC transporter ABCG36 is required for cadmium tolerance in rice. J. Exp. Bot. 2019, 70, 5909–5918. [Google Scholar] [CrossRef]
  61. Kang, J.; Hwang, J.U.; Lee, M.; Kim, Y.Y.; Assmann, S.M.; Martinoia, E.; Lee, Y. PDR-type ABC transporter mediates cellular uptake of the phytohormone abscisic acid. Proc. Natl. Acad. Sci. USA 2010, 107, 2355–2360. [Google Scholar] [CrossRef] [PubMed]
  62. Shimadzu, S.; Seo, M.; Terashima, I.; Yamori, W. Whole irradiated plant leaves showed faster photosynthetic induction than individually irradiated leaves via improved stomatal opening. Front. Plant Sci. 2019, 10, 1512. [Google Scholar] [CrossRef] [PubMed]
  63. He, Y.; Xu, J.; Wang, X.; He, X.; Wang, Y.; Zhou, J.; Zhang, S.; Meng, X. The Arabidopsis pleiotropic drug resistance transporters PEN3 and PDR12 mediate camalexin secretion for resistance to Botrytis cinerea. Plant Cell 2019, 31, 2206–2222. [Google Scholar] [CrossRef]
  64. Gutjahr, C.; Radovanovic, D.; Geoffroy, J.; Zhang, Q.; Siegler, H.; Chiapello, M.; Casieri, L.; An, K.; An, G.; Guiderdoni, E.; et al. The half-size abc transporters STR1 and STR2 are indispensable for mycorrhizal arbuscule formation in rice. Plant J. 2012, 69, 906–920. [Google Scholar] [CrossRef]
  65. Ko, D.; Kang, J.; Kiba, T.; Park, J.; Kojima, M.; Do, J.; Kim, K.Y.; Kwon, M.; Endler, A.; Song, W.Y.; et al. Arabidopsis ABCCG14 is essential for the root-to-shoot translocation of cytokinin. Proc. Natl. Acad. Sci. USA 2014, 111, 7150–7155. [Google Scholar] [CrossRef] [PubMed]
  66. Zhao, J.; Yu, N.; Ju, M.; Fan, B.; Zhang, Y.; Zhu, E.; Zhang, M.; Zhang, K. Abc transporter OsABCG18 controls the shootward transport of cytokinins and grain yield in rice. J. Exp. Bot. 2019, 70, 6277–6291. [Google Scholar] [CrossRef] [PubMed]
  67. Zhang, Y.; Kilambi, H.V.; Liu, J.; Bar, H.; Lazary, S.; Egbaria, A.; Ripper, D.; Charrier, L.; Belew, Z.M.; Wulff, N.; et al. ABC homeostasis and long-distance translocation are redundantly regulated by ABCG ABC importers. Sci. Adv. 2021, 7, eabf6069. [Google Scholar] [CrossRef] [PubMed]
  68. Kuromori, T.; Sugimoto, E.; Shinozaki, K. Arabidopsis mutants of AtABCG22, an ABC transporter gene, increase water transpiration and drought susceptibility. Plant J. 2011, 67, 885–894. [Google Scholar] [CrossRef]
  69. Kuromori, T.; Miyaji, T.; Yabuuchi, H.; Shimizu, H.; Sugimoto, E.; Kamiya, A.; Moriyama, Y.; Shinozaki, K. ABC transporter AtABCG25 is involved in abscisic acid transport and responses. Proc. Natl. Acad. Sci. USA 2010, 107, 2361–2366. [Google Scholar] [CrossRef]
  70. Liu, C.; Li, Z.; Tian, D.; Xu, M.; Pan, J.; Wu, H.; Wang, C.; Otegui, M.S. AP1/2 beta-mediated exocytosis of tapetum-specific transporters is required for pollen development in Arabidopsis thaliana. Plant Cell 2022, koac192. [Google Scholar] [CrossRef]
  71. Borghi, L.; Kang, J.; Ko, D.; Lee, Y.; Martinoia, E. The role of ABCG-type ABC transporters in phytohormone transport. Biochem. Soc. Trans. 2015, 43, 924–930. [Google Scholar] [CrossRef] [PubMed]
  72. Liu, S.; Li, Z.; Wu, S.; Wan, X. The essential roles of sugar metabolism for pollen development and male fertility in plants. Crop J. 2021, 9, 1223–1236. [Google Scholar] [CrossRef]
  73. Wan, X.; Wu, S.; Li, Z.; An, X.; Tian, Y. Lipid metabolism: Critical roles in male fertility and other aspects of reproductive development in plants. Mol. Plant 2020, 13, 955–983. [Google Scholar] [CrossRef] [PubMed]
  74. Wan, X.; Wu, S.; Li, Z.; Dong, Z.; An, X.; Ma, B.; Tian, Y.; Li, J. Maize genic male-sterility genes and their applications in hybrid breeding: Progress and perspectives. Mol. Plant 2019, 12, 321–342. [Google Scholar] [CrossRef]
  75. Jiang, Y.; An, X.; Li, Z.; Yan, T.; Zhu, T.; Xie, K.; Liu, S.; Hou, Q.; Zhao, L.; Wu, S.; et al. CRISPR/Cas9-based discovery of maize transcription factors regulating male sterility and their functional conservation in plants. Plant Biotechnol. J. 2021, 19, 1769–1784. [Google Scholar] [CrossRef] [PubMed]
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Figure 1. Genomic distribution of the 51 ZmABCG genes in maize chromosomes. Chromosome number and genomic length are indicated at the top and bottom of each chromosome, respectively. The physical location of each ZmABCG gene is indicated to the right of chromosomes. Mb, million base pair.
Figure 1. Genomic distribution of the 51 ZmABCG genes in maize chromosomes. Chromosome number and genomic length are indicated at the top and bottom of each chromosome, respectively. The physical location of each ZmABCG gene is indicated to the right of chromosomes. Mb, million base pair.
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Figure 2. Phylogenetic analysis of ABCGs in maize, rice and Arabidopsis. (A) Gene structures of half-size and full-size ABCG. NBD, nucleotide binding domain; TMD, transmembrane domain; (B) Phylogenetic analysis of ABCGs in maize (51), rice (54) and Arabidopsis (43). Subgroup 1 contains 90 half-size ABCGs, including 31 in maize, 31 in rice and 28 in Arabidopsis. Subgroup 2 consists of 58 full-size ABCGs, including 20 in maize, 23 in rice and 15 in Arabidopsis. Subgroups 1 and 2 can be classified into 5 and 3 clades, respectively. Stars indicate the ABCGs involved in male sterility.
Figure 2. Phylogenetic analysis of ABCGs in maize, rice and Arabidopsis. (A) Gene structures of half-size and full-size ABCG. NBD, nucleotide binding domain; TMD, transmembrane domain; (B) Phylogenetic analysis of ABCGs in maize (51), rice (54) and Arabidopsis (43). Subgroup 1 contains 90 half-size ABCGs, including 31 in maize, 31 in rice and 28 in Arabidopsis. Subgroup 2 consists of 58 full-size ABCGs, including 20 in maize, 23 in rice and 15 in Arabidopsis. Subgroups 1 and 2 can be classified into 5 and 3 clades, respectively. Stars indicate the ABCGs involved in male sterility.
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Figure 3. The main functions of ABCG transporters in Arabidopsis, rice and maize. (A) The proposed working model of ABCG transporters involved in anther and pollen development. Several ABCGs transfer tapetum-generated lipidic and other precursors for anther cuticle and pollen wall development, and AtABCG28 is required for the apical accumulation of reactive oxygen species in growing pollen tubes. AtG, AtABCG; Ba, baculum; Cu, cuticle; C/W, cutin and wax; Ep, epidermis; En, endothecium; In, intine; Ip, intine precursors; MI, membrane lipids; ML, middle layer; Ne, nexine; Np, nexine precursors; Pm, plasma membrane; Sp, sporopollenin precursors; SV, secretory vesicle; Ta, tapetum; Te, tectum; TGN, trans-Golgi network; Ty, tryphine; Tp, tryphine precursors; ZmG, ZmABCG. (B) The working model of ABCG transporters contributed to the formation of a tight cuticle layer and vascular development in Arabidopsis. The homodimers of AtABCG5/AtABCG5, AtABCG11/AtABCG11, and AtABCG13/AtABCG13, and the heterodimers of AtABCG11/AtABCG5 and AtABCG11/AtABCG12 transfer wax/cutin components for the formation of tight cuticle layers. The homodimers of AtABCG11/AtABCG11 and AtABCG9/AtABCG9, and the heterodimers of AtABCG11/AtABCG9 and AtABCG11/AtABCG14 transport vascular components for vascular development. Cu, cuticle; CW, cell wall; PM, plasma membrane. (C) Regulation of plant resistance by ABCG transporters in response to biotic and abiotic factors. The stress factors, ABCG transporters and their corresponding substrates and physiological roles in plants, are displayed in (C). ABA, abscisic acid; SLs, strigolactones. (D) Hormone transport and signaling of ABCG transporters. The hormone, ABCG transporters and their biological functions are displayed in (D). CKs, cytokinins; ABA, abscisic acid; Aux, Auxin; IBA, indole-3-butyric acid; JA, jasmonic acid; JA-Ile, jasmonic acid-isoleucine.
Figure 3. The main functions of ABCG transporters in Arabidopsis, rice and maize. (A) The proposed working model of ABCG transporters involved in anther and pollen development. Several ABCGs transfer tapetum-generated lipidic and other precursors for anther cuticle and pollen wall development, and AtABCG28 is required for the apical accumulation of reactive oxygen species in growing pollen tubes. AtG, AtABCG; Ba, baculum; Cu, cuticle; C/W, cutin and wax; Ep, epidermis; En, endothecium; In, intine; Ip, intine precursors; MI, membrane lipids; ML, middle layer; Ne, nexine; Np, nexine precursors; Pm, plasma membrane; Sp, sporopollenin precursors; SV, secretory vesicle; Ta, tapetum; Te, tectum; TGN, trans-Golgi network; Ty, tryphine; Tp, tryphine precursors; ZmG, ZmABCG. (B) The working model of ABCG transporters contributed to the formation of a tight cuticle layer and vascular development in Arabidopsis. The homodimers of AtABCG5/AtABCG5, AtABCG11/AtABCG11, and AtABCG13/AtABCG13, and the heterodimers of AtABCG11/AtABCG5 and AtABCG11/AtABCG12 transfer wax/cutin components for the formation of tight cuticle layers. The homodimers of AtABCG11/AtABCG11 and AtABCG9/AtABCG9, and the heterodimers of AtABCG11/AtABCG9 and AtABCG11/AtABCG14 transport vascular components for vascular development. Cu, cuticle; CW, cell wall; PM, plasma membrane. (C) Regulation of plant resistance by ABCG transporters in response to biotic and abiotic factors. The stress factors, ABCG transporters and their corresponding substrates and physiological roles in plants, are displayed in (C). ABA, abscisic acid; SLs, strigolactones. (D) Hormone transport and signaling of ABCG transporters. The hormone, ABCG transporters and their biological functions are displayed in (D). CKs, cytokinins; ABA, abscisic acid; Aux, Auxin; IBA, indole-3-butyric acid; JA, jasmonic acid; JA-Ile, jasmonic acid-isoleucine.
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Figure 4. Expression analysis of ABCG genes in maize. (A) Expression analysis of 51 ABCG genes in maize based on RNA-seq data in maize inbred lines W23, B73, Oh43 and Zheng58. These genes are clustered into two clusters. Genes in cluster I were clustered into four sub-clusters. (B) qPCR analysis of 15 ABCG genes from sub-clusters I-1, I-2, and cluster II in developing anthers from stages 5 to 13 (S5–S13). Data are means ± SD, n = 3.
Figure 4. Expression analysis of ABCG genes in maize. (A) Expression analysis of 51 ABCG genes in maize based on RNA-seq data in maize inbred lines W23, B73, Oh43 and Zheng58. These genes are clustered into two clusters. Genes in cluster I were clustered into four sub-clusters. (B) qPCR analysis of 15 ABCG genes from sub-clusters I-1, I-2, and cluster II in developing anthers from stages 5 to 13 (S5–S13). Data are means ± SD, n = 3.
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Table
Table 1. The maize ABCG Subfamily: new nomenclature based on B73 reference genome V4.0 and pre-existing synonyms.
Table 1. The maize ABCG Subfamily: new nomenclature based on B73 reference genome V4.0 and pre-existing synonyms.
No.New NameSynonyms 1Gene Models
(B73 V4)		Chr.Length (aa)Expression Organs 2
RootMeristemLeaveInternodeTasselAntherCobSilkSeedEmbryo
1ZmABCG1ABC-2Zm00001d0277231753 + +
2ZmABCG2ABCG2Zm00001d0286891790 + +
3ZmABCG3ABCG11Zm00001d0326011736 ++++ +++
4ZmABCG4ABCG24Zm00001d0328551883++++++ +++
5ZmABCG5ABCG3Zm00001d03491811078++++++ +++
6ZmABCG6ABCG11Zm00001d0028712721 +++ +++
7ZmABCG7ABCG25Zm00001d0047622632++++
8ZmABCG8ABCG6Zm00001d0429533761+ + +
9ZmABCG9ABCG25Zm00001d0437223738 +++
10ZmABCG10ABCG10Zm00001d0444763609+ + +
11ZmABCG11ABCG11Zm00001d0486214720 + + + +
12ZmABCG12-Zm00001d0530494636++++ +++
13ZmABCG13ABCG2Zm00001d0139605710 ++++++++
14ZmABCG14ABCG24Zm00001d01850051112 +
15ZmABCG15ABCG16Zm00001d0355536714++++++ ++
16ZmABCG16-Zm00001d0380686694+ + +
17ZmABCG17-Zm00001d0193987693+ +++
18ZmABCG18ABCG11Zm00001d0208117736+ + +
19ZmABCG19ABC-2Zm00001d0085128695 ++++ ++++
20ZmABCG20-Zm00001d0094928275++++ + ++
21ZmABCG21-Zm00001d0104268690 +++++ ++
22ZmABCG22-Zm00001d0110068712++++++ +++
23ZmABCG23ABCG10Zm00001d0113508507+ +
24ZmABCG24ABCG16Zm00001d0124388743+ + +
25ZmABCG25-Zm00001d0448959618+++++++ ++
26ZmABCG26ABCG28Zm00001d04606891040 +
27ZmABCG27ms2Zm00001d0465379676+ +++ ++++
28ZmABCG28-Zm00001d02407510892 + + +
29ZmABCG29-Zm00001d02449710727+++++ + +
30ZmABCG30ABCG24Zm00001d025031101101+++++ +
31ZmABCG31-Zm00001d02670610750++++++ +++
32ZmABCG32-Zm00001d03172411357 + + +
33ZmABCG33-Zm00001d03494011490+++++ +++
34ZmABCG34ABCG51Zm00001d00335421425 ++ ++
35ZmABCG35glossy13Zm00001d03963131425 ++ +++ +
36ZmABCG36ABCG38Zm00001d04359831488+ + +
37ZmABCG37-Zm00001d04444231574+ +++ ++
38ZmABCG38ABCG37Zm00001d04444331448+ + +
39ZmABCG39ABCG39Zm00001d04886041446+ ++ +++
40ZmABCG40ABCG45Zm00001d05272641237+
41ZmABCG41ABCG39Zm00001d05361241443+ +++
42ZmABCG42ABCG42Zm00001d03698661508+ + + +
43ZmABCG43ABCG45Zm00001d01995171224+
44ZmABCG44-Zm00001d01996171056+ ++
45ZmABCG45ABCG53Zm00001d02013471451+ + +
46ZmABCG46ABCG43Zm00001d02164771445+ ++
47ZmABCG47ABCG36Zm00001d01131581439+ ++ ++ +
48ZmABCG48ABCG37Zm00001d01131981449+
49ZmABCG49ABCG42Zm00001d04627791540+ +++
50ZmABCG50ABCG41Zm00001d023392101472+
51ZmABCG51ABCG48Zm00001d025012101465+ ++ +
Notes: 1. Synonyms were retrieved from MaizeGDB (www.maizegdb.org (accessed on 8 May 2022)) and NCBI (https://www.ncbi.nlm.nih.gov/ (accessed on 8 May 2022)); 2. Expression information of maize ABCG genes was retrieved from MaizeGDB (www.maizegdb.org (accessed on 20 April 2022)).
Table
Table 2. Functional Classifications of The Reported ABCG Genes in Arabidopsis, Rice and Their Orthologs in Maize.
Table 2. Functional Classifications of The Reported ABCG Genes in Arabidopsis, Rice and Their Orthologs in Maize.
No.Gene NameGene IDMaize OrthologExpression OrganBiological FunctionReference
I. Anther development and male fertility
1AtABCG11AT1G17840ZmABCG13
ZmABCG3
ZmABCG6		Stems; Leaves; Roots; Inflorescences; Flowers; Seeds; SiliquesFlower cutin and root suberin formation; Vascular development.[17,25,26]
2OsABCG26Os10g0494300ZmABCG13
ZmABCG3		Anthers; PistilsAnther cuticle and pollen exine formation and pollen-pistil interaction[18,19]
3ZmMs13/
ZmABCG13 *		Zm00001d013960-AnthersCallose dissolution; Anther cuticle and pollen exine formation[7]
4AtABCG26AT3G13220ZmABCG27Anthers; Siliques; Leaves; StemsExine formation[12,13,14]
5OsABCG15Os06g0607700ZmABCG27AnthersExine formation and pollen development[15,16,19]
6ZmMs2/
ZmABCG27 **		Zm00001d046537-AnthersTransport of anther cutin and wax components[8,10]
7AtABCG1At2G39350ZmABCG2Roots; Flowers; Stamens; Pistils; Seedlings; Leaves; Shoot meristemsMale gametophyte development; Pollen tube growth; Suberin formation in roots.[20,21,22,27]
8AtABCG16AT3G55090ZmABCG2Cotyledons; Roots; Seeds; Flowers; LeavesMale gametophyte development and pollen tube growth; Anther filament; JA and ABA responses; Plant pathogen response.[20,21,22,28,29]
9OsABCG3/
LSP1		Os01g0836600ZmABCG24
ZmABCG8		AnthersNormal pollen fertility and pollen wall formation[23,24]
10AtABCG9AT4G27420ZmABCG29Cotyledons; Leaves; Stamen; Siliques; Roots; AnthersSterol accumulated on pollen surface; Proper vascular development[11,25]
11AtABCG31AT2G29940ZmABCG34Inflorescences; Anthers; Rosette leaves; Stems; Seedlings; SiliquesSterol accumulation on pollen surface; ABA export from endosperm; Seed germination; Disease response[11,30]
12AtABCG28AT5G60740ZmABCG26
ZmABCG14		Pollen tubes; Pollen grainsPolyamine and ROS translocation at the growing tip of pollen tube[31]
II. Vegetative and female organ development
1AtABCG2AT2G37360ZmABCG2Roots; Seedlings; AnthersSuberin barrier synthesis in roots and seed coats[21]
2AtABCG6AT5G13580ZmABCG2Roots; Seeds; AnthersSuberin barrier synthesis in roots and seed coats[21]
3AtABCG20/
AtAwake1		AT3G53510ZmABCG2Roots; Seedings and anthersSuberin barrier synthesis in roots and seed coats; Seed dormancy[21,32]
4AtABCG5AT2G13610ZmABCG31Cotyledons; Roots; ShootsWax precursor transport; Shoot branching; Root suberization [33,34,35]
5AtABCG12AT1G51500ZmABCG21Stems; Leaves; Siliques; Flowers; RootsCuticle formation; Wax secretion; Abiotic stress response[26,36]
6AtABCG13AT1G51460ZmABCG21Flowers; Leaves; Stems; Siliques; RootsFlower cuticular lipids transport[37,38]
7AtABCG21AT3G25620ZmABCG29Seedlings; LeavesStomatal regulation[39]
8AtABCG27AT3G52310ZmABCG1Flowers; Pistils; LeavesCellulose synthesis; Flower and leaf development[40,41]
9AtABCG29AT3G16340ZmABCG36Roots; Stems; Leaves; Anthers; Siliques; SeedingsLignin biosynthesis[40,42]
10AtABCG32AT2G26910ZmABCG35Leaves; Stems; Flowers; Seedlings; SiliquesCuticular layer of the cell wall formation[43,44]
11OsABCG31Os01g0177900ZmABCG35LeavesCuticle formation[45]
12AtABCG33AT2G37280ZmABCG50Stems; RootsCellulose synthesis; Lignification[40,46]
13AtABCG34AT2G36380ZmABCG46
ZmABCG33
ZmABCG51		Roots; LeavesCamalexin secretion to leaf surface and thereby prevents A. brassicicola infection; Root exudation[47]
14AtABCG37AT3G53480ZmABCG50Roots; SeedlingsIBA transported out of the cells; Secretion of scopoletin and derivatives[48,49]
15ZmGL13Zm00001d039631-LeavesNecrotic glossy leaf; Plants smaller than nonmutant sibs[9]
III. Biotic and abiotic stress response
1OsABCG5/
RCN1		Os03g0281900ZmABCG2Roots; Tiller buds; Basal part of stem; Leaves.Lateral shoot outgrowth; ABA accumulation in guard cells under drought stress; Root hypodermis suberization[34,35,50]
2AtABCG19AT3G55130ZmABCG2Leaves; Roots; Flowers; SeedingsKanamycin resistance; Zinc homeostasis; Nicotianamine transport[51,52]
3OsABCG9Os04g0528300ZmABCG6Seminal roots; Young shoots; Anthers; StemsCuticular permeability and drought sensitivity [53]
4OsABCG43Os07g0522500ZmABCG46RootsCd tolerance in yeast[54]
5AtABCG35AT1G15210ZmABCG36RootsRoot exudation; Cadmium response[55,56]
6AtABCG36AT1G59870ZmABCG36Roots; Leaves; hydathodes; Stems; Inflorescences; Flowers; SiliquesAn efflux pump of Cd2+ or Cd conjugates; Drought and salt resistance; IBA Transport; Root and cotyledon development[57,58,59]
7OsABCG36Os01g0609300ZmABCG36Roots; ShootsCadmium tolerance; Heavy metal stress[60]
8AtABCG40AT1G15520ZmABCG41/
ZmABCG39		Inflorescences; Flowers; Roots; Leaves; Stems; Seeds; SiliquesStomatal regulation and ABA importation; Seed germination; Pathogen and drought response[30,61,62,63]
9OsSTR1Os09g0401100ZmABCG28Roots; Panicles; Leaves; Stems; EmbryosMycorrhizal arbuscule formation[64]
10OsSTR2Os07g0191600-
IV. Hormone transport and signaling
1AtABCG14AT1G31770ZmABCG29Cotyledons; Rosette leaves; Flowers; Roots; SiliquesVascular development; Cytokinin translocation in shoot[25,65]
2OsABCG18Os08g0167000ZmABCG29Roots; Stems; Leaves; PaniclesLong-distance transport of cytokinin in shoot and promote grain yield[66]
3AtABCG17AT3G55100ZmABCG2Roots; LeavesABA homeostasis and long-distance translocation[67]
4AtABCG18AT3G55110
5AtABCG22AT5G06530ZmABCG1Seedlings; Roots; Stems; Leaves; FlowersStomatal regulation; ABA signaling; Lignification[39,40,68]
6AtABCG25AT1G71960ZmABCG12/
ZmABCG7		Seedlings; Roots; Stems; Leaves; FlowersStomatal regulation; ABA export from endosperm; Seed germination[30,62,69]
7AtABCG30AT4G15230ZmABCG50Roots; SeedsABA import into the embryo; Seed germination; Monolignol transport[30,55]
Notes: At, Arabidopsis; Os, rice; Zm, Maize. * Previously named as ZmABCG2a; ** previously named as ZmABCG26. II. 16–18, AtABCG1, AtABCG9, and AtABCG11 are also involved in vegetative and female organ development. IV. 8-13, AtABCG31, AtABCG36, AtABCG37, AtABCG40 and OsABCG5/RCN1 are also involved in hormone response.
Table
Table 3. The Substrate Identification of Plant ABCG Transporters.
Table 3. The Substrate Identification of Plant ABCG Transporters.
No.TransportersTypesSubstrate(s)Method of Substrate IdentificationReference
I. Isotope labelling experiment in vivo
1AtABCG11Half-size10,16-diOH C16:0-2-glycerol; ω-OH C16:0[3H]-10,16-diOH C16:0-2-glycerol; [14C]-u-OH C16:0 export assay using N. benthamiana protoplast system[44]
2AtABCG14Half-sizeCytokininsWT and atabcg14 mutant cultivated in 14C-labeled trans-zeatin (tZ) medium[65]
3AtABCG16Half-sizeJasmonate3H-JA transport of yeast strain expressing AtABCG16; transport of 3H-JA and 3H-JA-Ile by the nuclei isolated from abcg16 plant[28]
4AtABCG25Half-sizeABA3H-ABA transport of yeast strains expressing AtABCG25[30,69]
5AtABCG30Full-sizeABA3H-ABA transport of yeast strains expressing AtABCG30[30]
6AtABCG31Full-sizeABA3H-ABA transport of yeast strains expressing AtABCG31[30]
7AtABCG32Full-size10,16-diOH C16:0-2-glycerol; ω-OH C16:0; C16:0 DCA[3H]-10,16-diOH C16:0-2-glycerol; [14C]-u-OH C16:0; [14C]-C16:0 DCA export assay using N. benthamiana protoplast system[44]
8AtABCG37Full-sizeAuxin precursor indole-3-butyric acid (IBA)3H-IBA export from abcg37 leaf mesophyll protoplasts; 3H-IBA transport in yeast strains expressing AtABCG37; export of 3H-2,4-D and 3H-IBA in HeLa cells expressing AtABCG37[49]
9AtABCG40Full-sizeABA3H-ABA uptake in yeast strain YMM12 and BY-2 cell lines expressing AtABCG40[30]
II. Substance analysis using the GC-MS system
1AtABCG2Half-sizeSuberin precursorsSuberin monomers analysis by using GC-MS system[21]
2OsABCG5/
RCN1		Half-sizeABA; suberin monomersPhenotypic and expression analysis of RCN1 in WT and RCN1-RNAi plants treated with ABA; Histochemical staining and suberin contents analysis by GC-MS[34,35,50]
3AtABCG5Half-sizeCutin/wax precursorsSubstance analysis by using GC-MS[33]
4AtABCG6Half-sizeFatty acids; Fatty alcoholsSuberin monomers analysis by using GC-MS[21]
5AtABCG9Half-sizeSteryl glycosidesSubstance analysis by using GC-MS[11]
6OsABCG9Half-sizeWax precursorsSubstance analysis by using GC-MS[53]
7OsABCG26Half-sizeAnther cuticular wax and cutin monomersSubstance analysis by using GC-MS[18,19]
8ZmMS13/
ZmABCG13		Half-sizeAnther cuticular wax and cutin monomersSubstance analysis by using GC-MS[7]
9AtABCG12Half-sizeLipids; Wax componentsSubstance analysis by using GC-MS[26,36]
10AtABCG13Half-sizeCuticular lipidsSubstance analysis by using GC-MS[37]
11AtABCG20/
Awake1		Half-sizeSuberin precursors; Fatty acidsSubstance analysis by using GC-MS[21,32]
12AtABCG26Half-sizeSporopollenin precursors; PolyketidesSubstance analysis by using GC-MS[12,14]
13OsABCG15Half-sizeSporopollenin and cutin precursorsSubstance analysis by using GC-MS[15,16]
14ZmMS2/
ABCG26		Half-sizeSporopollenin and cutin precursorsSubstance analysis by using GC-MS[8,10]
15OsABCG31Full-sizeCutin precursorsSubstance analysis by using GC-MS[45]
III. Other methods
1AtABCG1Half-sizeFatty alcohols; Fatty acidsAtABCG1 protein purified in Pichia pastoris to test its ATPase assay[27]
2ZmMS13/
ZmABCG13		Half-sizeFatty alcohols; Fatty acidsZmMS13 protein purified in E. coli and its ATPase assay in vitro[7]
3OsABCG18Half-sizeCytokininsExport assay with OsABCG18 expressing N. benthamiana protoplasts[66]
4OsABCG3/
LSP1		Half-sizePollen wall and coat materialsPhenotypic and qRT-PCR analysis of WT and osabcg3 mutant[23,24]
5AtABCG19Half-sizeKanamycinKanamycin treatment of AtABCG19-overexpressing plants[52]
6AtABCG22Half-sizeABA; lignin precursorsSpeculation according to the same phenotype with AtABCG21[40,68]
7AtABCG28Half-sizePolyamineImmunostaining of polyamines in pollen tubes[31]
8AtABCG29Full-sizep-coumaryl alcoholp-coumaryl alcohol uptake using microsomes from S. cerevisiae expressing AtABCG29[42]
9AtABCG34Full-sizeCamalexinCamalexin toxicity assay in Arabidopsis and BY2 cells expressing AtABCG34[47]
10OsABCG43Full-sizeCdCd inducible and confers Cd tolerance on OsABCG43-expressing yeast cell.[54]
11AtABCG36Full-sizeLignin precursors; Cd; IBAThe atabcg36 mutants and WT were tested in IBA-containing agar medium under yellow filtered light conditions.[57,59]
12OsABCG36Full-sizeCd2+Efflux transport of Cd in OsABCG36-expressing yeast cell.[60]
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Wu, S.; Fang, C.; Li, Z.; Wang, Y.; Pan, S.; Wu, Y.; An, X.; Long, Y.; Wan, X. ATP-Binding Cassette G Transporters and Their Multiple Roles Especially for Male Fertility in Arabidopsis, Rice and Maize. Int. J. Mol. Sci. 2022, 23, 9304. https://doi.org/10.3390/ijms23169304

AMA Style

Wu S, Fang C, Li Z, Wang Y, Pan S, Wu Y, An X, Long Y, Wan X. ATP-Binding Cassette G Transporters and Their Multiple Roles Especially for Male Fertility in Arabidopsis, Rice and Maize. International Journal of Molecular Sciences. 2022; 23(16):9304. https://doi.org/10.3390/ijms23169304

Chicago/Turabian Style

Wu, Suowei, Chaowei Fang, Ziwen Li, Yanbo Wang, Shuangshuang Pan, Yuru Wu, Xueli An, Yan Long, and Xiangyuan Wan. 2022. "ATP-Binding Cassette G Transporters and Their Multiple Roles Especially for Male Fertility in Arabidopsis, Rice and Maize" International Journal of Molecular Sciences 23, no. 16: 9304. https://doi.org/10.3390/ijms23169304

APA Style

Wu, S., Fang, C., Li, Z., Wang, Y., Pan, S., Wu, Y., An, X., Long, Y., & Wan, X. (2022). ATP-Binding Cassette G Transporters and Their Multiple Roles Especially for Male Fertility in Arabidopsis, Rice and Maize. International Journal of Molecular Sciences, 23(16), 9304. https://doi.org/10.3390/ijms23169304

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