MATE Transporters Regulate Agronomic Traits

Version	Summary	Created by	Modification	Content Size	Created at	Operation
1		Hon-Ming Lam	--	3532	2022-04-29 11:23:55	\|
2	format correct	Vivi Li	Meta information modification	3532	2022-05-05 03:24:28	\|

This entry is adapted from the peer-reviewed paper 10.3390/agronomy12040878

Multidrug and toxic compound extrusion (MATE) transporters are ancient proteins conserved among various kingdoms, from prokaryotes to eukaryotes. In plants, MATEs usually form a large family in the genome. Homologous MATE transporters have different subcellular localizations, substrate specificities, and responses to external stimuli for functional differentiations. The substrates of MATEs in plants include polyphenols, alkaloids, phytohormones, and ion chelators. The accumulation of these substrates is often associated with favorable agronomic traits such as seed and fruit colors, the balance between dormancy and germination, taste, and stress adaptability. In crops, wild germplasms and domesticated germplasms usually have contrasting agronomic traits such as seed color, seed taste, and stress tolerance. MATE transporters are involved in the regulations of these traits.

ancient protein gene family multidrug and toxic compound extrusion (MATE) transporter agronomic trait domesticated crop wild crop

1. Introduction

Multidrug and toxic compound extrusion (MATE) transporters are ancient proteins conserved among the three domains of life: Bacteria, Archaea, and Eukarya. In plants, MATE transporters usually form large families with dozens to over a hundred family members ^[1]^[2]^[3]^[4]^[5]^[6]^[7]^[8]. For example, 117 MATE genes were identified in the Glycine max genome, 49 in Zea mays ^[2], 67 in Solanum lycopersicum ^[6], 71 Populus trichocarpa ^[3], 53 in Oryza sativa ^[7], 56 in Arabidopsis thaliana ^[8], 40 in Medicago truncatula ^[4], 65 in Vitis vinifera ^[5], 48 in Solanum tuberosum ^[9], and 33 in Vaccinium corymbosum ^[10]. Within the same species, the copy numbers of MATE genes have often expanded due to genome duplication events ^[3]^[11].

A typical MATE transporter consists of 12 transmembrane domains (TMDs) and is driven by a H⁺ or Na⁺ gradient across the biological membrane ^[12]^[13]. In plants, MATE transporters are involved in growth, stress responses, leaf senescence, and metabolite transport including the efflux of antibiotics, the transportation and compartmentalization of alkaloids and flavonoids, iron homeostasis, aluminum tolerance, and the transportation of phytohormones ^[14]^[15]^[16]^[17]. MATE proteins have been reported to transport substrates that are characteristic to particular groups of plants. For example, the characteristic colored skin of berry fruit is known to be resulted from the accumulation of anthocyanins, while VvMATE1 and VvMATE2 were reported to be putative proanthocyanidin transporters in seed berries ^[18]. Another example is the rich content of isoflavone in soybean seeds ^[19]. GmMATE1, GmMATE2, and GmMATE4 were reported to mediate isoflavone transport into the vacuole ^[16]^[17]. As discussed in Section 1, genome-wide identification studies demonstrated that many plant species have a large family of MATE transporters. The multitasking abilities of MATE transporters in plants to mediate the transport of various substrates for the regulation of different biological processes, including xenobiotic detoxification, regulation of iron homeostasis, tolerance to aluminum, regulation of biotic stress, and phytohormone transport, have been reviewed ^[20]. The role of MATE transporter in exporting isoflavonoid for regulating nodulation was also reported ^[21]. The diversity of metabolites in different plant species and the capacities of MATEs to transport various substrates are the possible reasons behind the large MATE families in plants.

Most eukaryotic MATE transporters mediate substrate transports in exchange for H⁺ from the other side of the biological membrane ^[13]. However, prokaryotic MATE transporters could utilize H⁺ or Na⁺ as the anti-porting agent ^[13]. Although MATE transporters are highly conserved in terms of the 12 typical MATE-type TMDs, they have different substrate specificities, such as ion chelators, phytohormones, alkaloids, and flavonoids ^[4]^[16]^[17]^[22]^[23]^[24]^[25]^[26]^[27]^[28]^[29]. Many agronomic traits, such as seed color, bitterness of seeds, stress tolerance, and the balance between dormancy and germination, are closely related to the functions of MATE transporters. Many of these agronomic traits regulated by MATE transporters display contrasting properties between wild crops and domesticated crops. For example, compared to wild germplasms, domesticated germplasms usually have less colored seeds, bitter seeds, and easier germination of seeds ^[30]^[31]^[32]. On the other hand, some domesticated germplasms contain higher levels of alkaloids compared to wild germplasms due to different cultivation purposes ^[33]^[34]. Some domesticated germplasms may also have improved stress tolerance compared to the wild germplasms ^[35]. Many of these favorable agronomic traits in domesticated germplasms are associated with metabolites transported by MATE transporters.

During domestication, specific alleles of domestication genes resulting in the desired agronomic traits were selected ^[36]^[37]. The artificial selection during domestication and breeding resulted in a drastic decrease of genetic diversity in certain regions of the genome, where the potentially beneficial alleles for domestication are located ^[38]. Examples of domestication genes include TB1 (Teosinte Branched 1), which encodes a transcriptional regulator for regulating apical dominance and leads to short and ear-tipped branches of domesticated maize ^[39]^[40], GmOLEO1, which encodes a oleosin protein for enhancing the seed oil content in domesticated soybean ^[41], and BH4 (BLACK HULL4), which encodes an amino acid transporter for the regulation of the hull color of rice ^[42]. The 22-bp deletion in the exon of BH4 resulted in the white hull color of cultivated rice ^[42]. Details of domestication genes have been summarized in previous reviews ^[43]^[44]. Although MATE genes have not been characterized as domestication genes, they are involved in regulating favorable traits, which are selected during domestication. The nature of MATEs being transporters to directly transport metabolites that bring forth the desirable traits, such as color and taste, may suggest MATE genes as the suitable candidate genes for molecular breeding to shape a particular trait.

2. Favorable Agronomic Traits

During cultivation, plants have been selected for improvements in yield and harvestability ^[45]. Other traits, such as seed color and fruit color ^[30]^[31], the balance between dormancy and germination ^[32], taste profile ^[46]^[47], and adaptability to the environment ^[48], are also constantly under conscious selection by breeders and consumers. MATE transporters are involved in the regulation of these agronomic traits.

2.1. Color

Seed coat color is usually distinguishable between wild germplasms and domesticated germplasms. During domestication, seeds with lighter color were selected due to the ease of sowing and religious reasons ^[30]. Common examples of such domesticated crop plants include legumes, rice, and sorghum. As reviewed previously, in legumes such as Phaseolus vulgaris, Lablab purpureus, Arachis hypogaea, soybean, Pisum sativum, lentil, and Cicer arietinum, the cultivars tend to have seed coats with lighter colors or less complex patterns compared to their wild relatives ^[46]. In rice, the change in grain color is one of the alterations due to domestication ^[49]. Wild rice grains usually have black hulls and red pericarps, while cultivated rice accessions usually have straw-white hulls. It was reported that such a change in hull color was due to a mutation in the gene Bh4, while the change in pericarp color was due to a mutation in the gene Rc. Various deletions in different regions of Bh4 resulted in the same straw-white hull phenotype in different domesticated rice accessions ^[49]. In Amaranth, the change in seed color from dark to white is also a contrasting trait between wild germplasms and domesticated germplasms ^[50]. A MYB-like protein, homologous to the MYB-type transcription factors identified in other species for regulating seed coat color, was suggested to have soft selective sweep ^[50]. The maize homolog determining seed coat color is known as Anthocyanin Regulatory C1 ^[50]. Similarly, domesticated quinoa accessions tend to have seeds of lighter colors, such as white, yellow, red, and purple, while wild quinoa accessions tend to have black seeds ^[51].

Major plant pigments include anthocyanins, betalains, carotenoids, and chlorophylls ^[52]. Anthocyanins have been known to be associated with the black color of the seed coat ^[53]. In a study on the polyphenol composition of the colored seed coat of five pulses, including Cicer arietinum L., Vicia faba L., Lens culinaris Medik., Pisum sativum L., and Phaseolus vulgaris L., anthocyanins were only detected in the black seed coat of Lens culinaris Medik and Phaseolus vulgaris L. but not in the seed coat of other colors, such as white, green, brown, beige, grey, maple (patterned), and dun (brown) ^[54]. Although anthocyanins were not detected in the black seed coat of the chickpea and faba bean, another class of colored compound, procyanidins, was detected in the black seed coat of the faba bean ^[54]. However, it was not clear which compounds result in the black seed coat color of the chickpea ^[54].

MATE transporters have been known to mediate the accumulation of colored compounds in the seed coat. For example, in Arabidopsis, TRANSPARENT TESTA12 (TT12), which encodes a MATE transporter, was reported to mediate the sequestration of proanthocyanidins (PAs) in the vacuole and thus enhance the accumulation of PAs in the seed coat ^[55]^[56]. In Medicago truncatula, MtMATE1 was reported to be functionally orthologous to Arabidopsis TT12, in mediating the vacuolar uptake of PAs and epicatechin 3′-O-glucoside, which is the precursor for PA biosynthesis (Zhao and Dixon, 2009). The mutation of MtMATE1 resulted in seeds with a lighter color compared to the wild type (Zhao and Dixon, 2009). In addition, the pale seed phenotype of the Arabidopsis tt12 mutant could be complemented by the ectopic expression of MtMATE1 (Zhao and Dixon, 2009). Later, it was found that Arabidopsis TT12 is regulated by TRANSPARENT TESTA GLABRA2 (TTG2), which encodes a WRKY-type transcription factor ^[22]. Compared to the wild type, the ttg2 mutant produces seeds with a lighter color ^[22]. Such a phenotype is consistent with the pale seed color resulting from the tt12 mutation (Zhao and Dixon, 2009).

Domesticated vegetables and fruits also have altered skin colors compared to the wild accessions. For example, wild carrots are usually white or off-white ^[57]^[58]. The edible part of carrot is the root, which grows underground. Having a colored root appears to offer no advantage to the plant’s growth and survival ^[57]. However, many domesticated carrots are colored, with roots in yellow, orange, red, and purple ^[57]^[58]^[59]. It was suggested that the first event of domestication resulted in the popularity of yellow and purple carrots ^[58]. After that, the second domestication event led to the popularity of the orange carrot ^[58]. The orange color is due to the accumulation of carotenes ^[58]. Another example is the grapevine (V. vinifera). The white and red fruits of the grapevine are preferred on the market, while the dark-colored ones of the wild ancestor are not as popular ^[31]. The pale green skin color of the domesticated grapevine fruit was reported to be due to a retroelement insertion in VvMybA1 and a mutation in VvMybA2, both of which encode MYB-type transcription factors ^[60]. The dark skin color of grapevine fruit is largely due to the accumulation of anthocyanins ^[31]. VvVHP1;2 (V. vinifera vacuolar H⁺ PPase 1;2) was reported to be the transcriptional activation target of VvMYBA1 ^[61]. The overexpression of VvVHP1;2 enhanced the accumulation of anthocyanins in transgenic berry fruit skins and transgenic Arabidopsis leaves ^[61]. The overexpression of VvVHP1;2 also led to the increased expression of VvMATE3 ^[61]. In V. vinifera, MATE transporters have been reported to mediate the accumulation of anthocyanins. anthoMATE1 and anthoMATE3 were reported to be tonoplast-localized MATE transporters that mediate the import of acylated anthocyanins in the vacuole ^[5]. In addition, VvMATE1 and VvMATE2, which localize in the membranes of the vacuole and Golgi, respectively, were reported to be associated with the transport of PAs ^[18].

Although MATE genes have not been regarded as domestication-related genes in crops, MATE transporters play important roles in regulating the color of seed and fruit, which have always been the agronomic traits selected. The link between the domesticated related genes, such as the MYB genes, and MATE transporters, which mediate the transport of colored compounds, has remained unclear. Nevertheless, MATE transporters that transport the colored compounds could be the possible candidates for molecular breeding when color is the agronomic trait of interest.

2.2. Dormancy

Seed dormancy is one of the contrasting traits between wild germplasms and domesticated germplasms ^[32]. Dormancy could prevent seeds from germinating under favorable conditions ^[62]. On the other hand, dormancy is critical for preventing preharvest sprouting when the humidity and temperature are favorable for germination ^[32]^[63]. Although a long dormancy is not desirable for cultivation, too short a dormancy causes problems such as preharvest sprouting and could result in low grain quality and quantity ^[63]. Therefore, an appropriate balance between seed dormancy and germination is a desirable trait selected during domestication. The equilibrium between ABA and GA levels regulates dormancy and the time for germination. Other phytohormones such as brassinosteroid, jasmonic acid, salicylic acid, cytokinin, strigolactone, and ethylene regulate the balance between ABA and GA ^[64]^[65]. In addition to ABA and GA, auxin is also recognized as a master regulator of dormancy for its role in regulating the expression of genes involved in dormancy and germination ^[65].

In Arabidopsis, the transport of ABA from maternal tissue to the embryo for dormancy regulation has been suggested ^[66]. In another report, it was shown that ABA is released from the endosperm to the embryo to regulate seed dormancy ^[67]. Later, ATP-binding cassette (ABC) transporters AtABCG25, AtABCG31, AtABCG30, and AtABCG40 were reported to be responsible for the transport of ABA from the endosperm to the embryo in Arabidopsis ^[68]. The mutation of AtABCG31, AtABCG30, or AtABCG40 led to a faster germination compared to the wild type ^[68].

Besides the ABC transporters mentioned above, in Arabidopsis, AtDTX50, a MATE transporter, was also identified as an ABA transporter that regulates seed dormancy ^[26]^[69]. AtDTX50 was found to be localized at the plasma membrane ^[26]. Using ectopic expressions of AtDTX50 in Escherichia coli cells and Xenopus oocytes, the ABA transportation activity of AtDTX50 was validated ^[26]. The Arabidopsis dtx50 mutant exhibited a slower germination rate when compared to the wild type upon the ABA treatment. This ABA-sensitive phenotype of the Atdtx50 mutant implies that this MATE transporter also plays a role in seed dormancy regulation ^[26].

2.3. Bitterness and Psychostimulant

2.3.1. Alkaloids

As reviewed previously, the taste of crops has been a character selected by breeders ^[46]^[47]. Domesticated crops tend to have reduced levels of alkaloids due to the bitter taste of alkaloids and the absence of selection pressure exerted by biotic stresses during domestication ^[46]^[47].

In Arabidopsis, AtDTX1 (Arabidopsis thaliana Detoxification 1) was identified to be a MATE-type transporter that mediates the transport of berberine, which confers a bitter taste ^[8]^[70]. The expression of AtDTX1 in E. coli mediated the efflux of berberine out of the bacterial cells ^[8]. A subcellular localization study demonstrated that AtDTX1 is localized in the plasma membrane ^[8]. Such exporter activity and plasma membrane localization of AtDTX1 are in line with a previous finding that alkaloids are transported between plant organs ^[71]. In Coptis japonica, which is a medicinal plant, the role of CjMATE1 in mediating berberine accumulation in vacuole was suggested ^[72]. CjMATE1 was found to localized at the tonoplast and preferably expressed in rhizomes, where berberine is accumulated ^[72]. Using yeast as a model, the berberine transport activity of CjMATE1 was shown ^[72]. Although berberine confers a bitter taste, which is an undesirable trait in most edible crops, it is of important pharmaceutical value in medicinal plants ^[73].

2.3.2. Cyanogenic Glucosides

Cyanogenic glucosides are plant metabolites that are related to defense mechanisms ^[74]. An example is domesticated sorghum (Sorghum bicolor), which produces high levels of cyanogenic glucosides when compared to its wild ancestors ^[34]. Sorghum bicolor contains a high level of cyanogenic compounds, which are bitter, and thus has been cultivated for forage crop and animal feed because of the bitter taste ^[34]^[75]. Young seedlings of domesticated Sorghum bicolor harbor high concentrations of cyanogenic glucosides, when compared to its wild relatives, including Sorghum brachypodum Lazarides, Sorghum bulbosum Lazarides, Sorghum ecarinatum Lazarides, Sorghum intrans F. Muell ex. Benth, Sorghum macrospermum E.D. Garber, and Sorghum matarankense E.D. Garber & L.A. Snyder ^[34]. Cyanogenic glucosides are derived from amino acids, such as L-valine, L-isoleucine, L-leucine, L-phenylalanine, and L-tyrosine, and synthesized by membrane-bound cytochrome P450s and UDP-glucosyl-transferase ^[74]. The synthesized cyanogenic glucosides would then be hydrolyzed by β-glucosidase into cyanohydrin, which is unstable, and would further dissociate to form hydrogen cyanide and ketone via a process known as cyanogenesis ^[74]. Cyanogenic glucosides are toxic to herbivores. During ingestion and chewing, cyanogenic glucosides confer a bitter taste with the release of toxic hydrogen cyanide, which leads to tissue disruption ^[74]. Young seedlings of sorghum plants are highly toxic ^[76]. Therefore, sorghum plants are usually grazed when the plants have reached the five-leaf stage where the toxicity is reduced ^[76]. Although toxic to herbivores, cyanogenic glucosides are beneficial to plants. They scavenge hydrogen peroxide, which is a reactive oxygen species, by the Radziszweski process to alleviate the oxidative stress caused by biotic and abiotic stresses ^[77]. In addition, cyanogenic glucosides, which are derived from amino acids, also serve as a primary means of nitrogen storage and transport, and as a nitrogen reservoir under adverse conditions ^[78]. During their domestication as a forage crop and animal feed, sorghum plants have been mainly grown under sub-optimal conditions such as in the dry tropics under high temperatures, in regions such as Africa and Australia ^[75]. Such adverse growth conditions probably drove the selection for high cyanogenic glucoside levels in domesticated sorghum. It was reported that the biosynthetic genes of cyanogenic glucosides are organized in a gene cluster to enhance the co-inheritance of alleles in the same biosynthetic pathway ^[79].

SbMATE2 was one of the genes found within the gene cluster encoding cyanogenic glucoside biosynthetic enzymes in the Sorghum bicolor genome ^[79]. It was found to be co-expressed with other cyanogenic glucoside biosynthetic genes ^[79]. A subcellular localization study demonstrated that SbMATE2 transporters localize at the vacuolar membrane ^[79]. The ability of SbMATE2 to transport cyanogenic glucosides, such as dhurrin and other hydroxynitrile glucosides, was demonstrated in the Xenopus laevis oocyte model ^[79]. The SbMATE2-mediated influx of cyanogenic glucosides into the vacuole was enhanced by a lower pH in the medium ^[79]. As MATE transporters utilize the proton gradient as a driving force, it was hypothesized that the direction of transport of cyanogenic glucosides by SbMATE2 is from the cytoplasm, where cyanogenic glucosides are synthesized, to the acidic vacuole ^[79]. Such storage of cyanogenic glucosides has been suggested as a strategy to reduce self-toxicity to the plant ^[79].

2.3.3. Nicotine

Besides food crops, tobacco (Nicotiana sp.), which is usually consumed as a psychostimulant, is also a popular plant known to have been domesticated. Unlike the general effort to reduce the levels of alkaloids in other food plants, human selection actually drives the increase in nicotine levels in tobacco. The use of tobacco by humans was estimated to have begun 12,300 years ago ^[80]. It was suggested that hunter-gatherers in western North America first cultivated wild tobacco ^[33]. Compared to wild tobacco plants, domesticated tobacco plants usually have larger leaves and higher levels of nicotine ^[33]. In Nicotiana tabacum, NtJAT1 (Nicotiana tabacum jasmonate-inducible alkaloid transporter 1), which is expressed in the leaf, stem, and root, mediates the efflux of nicotine out of the vacuole ^[29]. NtJAT2, which is also expressed in the leaf, was shown to have a similar nicotine export function to NtJAT1 when ectopically expressed in yeast ^[81]. Furthermore, NtMATE1 and NtMATE2 were reported to be localized in the tonoplast for the sequestration of nicotine from the vacuoles of root cells ^[82]. Nicotine is synthesized in the root and transported to the leaf ^[29]. Although the nicotine level in leaves could be enhanced by overexpressing transcription factors such as NtMYC2a and NtMYC2b, most nicotine synthetic genes, including NtPMT (Nicotiana tabacum putrescine N-methyltransferase), NtQPT (Nicotiana tabacum quinolinic acid phosphoribosyltransferase), NtMPO (Nicotiana tabacum N-methylputrescine oxidase), NtA622 (orphan oxidoreductase), NtBBL (Nicotiana tabacum berberine bridge enzyme-like), NtADC (Nicotiana tabacum arginine decarboxylase), and NtODC (Nicotiana tabacum ornithine decarboxylase), in NtMYC2a overexpressors were down-regulated ^[83]. Similar phenomena were reported in another study. The expression of NtMYC2a under constitutive promoters (GmUBI3 promoter/2XCaMV35S promoter) or a JA-inducible promoter (4XGAG) in tobacco plants led to the upregulation of nicotine level in the leaves ^[84]. Methyl-JA treatment further increased the nicotine level in transgenic plants expressing NtMYC2a under either one of these promoters ^[84]. It was also demonstrated that nicotine application at the root of tobacco seedlings repressed the expression levels of the nicotine synthetic genes regulated ^[83]. NtMYC2a and NtMYC2b form nuclear complexes with NtJAZ1, which is a transcriptional repressor of JA inducible genes, for the down-regulation of nicotine biosynthesis-related genes ^[85]. Considering that the whole profile of transcriptional regulatory targets of NtMYC2a and NtMYC2b are unclear, NtMYC2a- and NtMYC2b-mediated gene regulation involves JA signaling, which is associated with various physiological responses; the phenomenon that the nicotine level negatively regulates nicotine synthetic genes means MATE transporters that ultimately mediate the transport of nicotine in leaves may be the more direct candidates for altering the nicotine level.

3. MATE Transporters Are Possible Candidates for Molecular Breeding

Desirable traits in domesticated crops include light seed color for the ease of sowing and religious reasons ^[30]. Moreover, domesticated vegetable and wild vegetable tend to have contrasting color, with the fruits of domesticated vegetables usually being lighter in color ^[31]^[57]^[58]. In addition, domesticated crops have a better balance of dormancy and germination efficiency compared to wild crops to favor cultivation ^[32]^[63]. Domesticated crops may have less alkaloid level compared to wild crops due to the absence of biotic stresses as selective pressures ^[46]^[47]. To produce psychostimulants, domesticated tobacco has higher nicotine levels than wild tobacco ^[33]. To achieve the various favorable traits, the transports of substrates including pigmented metabolites, phytohormone, and alkaloids are involved.

4. Conclusions

MATE transporters are ancient proteins conserved among most species, from prokaryotes to eukaryotes. A special feature of MATEs is that they form a large gene family with many paralogous genes and/or large copy numbers in the same species. Such gene family member expansions were due to genome duplication events. The need to transport different substrates under different situations requires many homologous transporters and therefore results in a large gene family. MATEs mediate the transport of a wide variety of compounds, including those that give colors to various organs/tissues, flavor compounds, and phytohormones. As discussed above, many of these compounds had undergone selection during domestication. Although MATEs have seldom been discussed for their role in crop domestication, the involvement of MATEs in regulating domestication-related traits and the possibility of MATEs being candidates for molecular breeding should not be overlooked.

References

Liu, J.; Li, Y.; Wang, W.; Gai, J.; Li, Y. Genome-wide analysis of MATE transporters and expression patterns of a subgroup of MATE genes in response to aluminum toxicity in soybean. BMC Genom. 2016, 17, 223.
Zhu, H.; Wu, J.; Jiang, Y.; Jin, J.; Zhou, W.; Wang, Y.; Han, G.; Zhao, Y.; Cheng, B. Genomewide analysis of MATE-type gene family in maize reveals microsynteny and their expression patterns under aluminum treatment. J. Genet. 2016, 95, 691–704.
Li, N.; Meng, H.; Xing, H.; Liang, L.; Zhao, X.; Luo, K. Genome-wide analysis of MATE transporters and molecular characterization of aluminum resistance in Populus. J. Exp. Bot. 2017, 68, 5669–5683.
Zhao, J.; Dixon, R.A. MATE transporters facilitate vacuolar uptake of epicatechin 3’-O-glucoside for proanthocyanidin biosynthesis in Medicago truncatula and Arabidopsis. Plant Cell 2009, 21, 2323–2340.
Gomez, C.; Terrier, N.; Torregrosa, L.; Vialet, S.; Fournier-Level, A.; Verries, C.; Souquet, J.-M.; Mazauric, J.-P.; Klein, M.; Cheynier, V.; et al. Grapevine MATE-type proteins act as vacuolar H+-dependent acylated anthocyanin transporters. Plant Physiol. 2009, 150, 402–415.
dos Santos, A.L.; Chaves-Silva, S.; Yang, L.; Maia, L.G.S.; Chalfun-Júnior, A.; Sinharoy, S.; Zhao, J.; Benedito, V.A. Global analysis of the MATE gene family of metabolite transporters in tomato. BMC Plant Biol. 2017, 17, 185.
Tiwari, M.; Sharma, D.; Singh, M.; Tripathi, R.D.; Trivedi, P.K. Expression of OsMATE1 and OsMATE2 alters development, stress responses and pathogen susceptibility in Arabidopsis. Sci. Rep. 2014, 4, 3964.
Li, L.; He, Z.; Pandey, G.K.; Tsuchiya, T.; Luan, S. Functional cloning and characterization of a plant efflux carrier for multidrug and heavy metal detoxification. J. Biol. Chem. 2002, 277, 5360–5368.
Li, Y.; He, H.; He, L.-F. Genome-wide analysis of the MATE gene family in potato. Mol. Biol. Rep. 2019, 46, 403–414.
Chen, L.; Liu, Y.; Liu, H.; Kang, L.; Geng, J.; Gai, Y.; Ding, Y.; Sun, H.; Li, Y. Identification and expression analysis of MATE genes involved in flavonoid transport in blueberry plants. PLoS One 2015, 10, e0118578.
Maron, L.G.; Guimarães, C.T.; Kirst, M.; Albert, P.S.; Birchler, J.A.; Bradbury, P.J.; Buckler, E.S.; Coluccio, A.E.; Danilova, T.V.; Kudrna, D.; et al. Aluminum tolerance in maize is associated with higher MATE1 gene copy number. Proc. Natl. Acad. Sci. USA 2013, 110, 5241–5246.
Piddock, L.J.V. Clinically relevant chromosomally encoded multidrug resistance efflux pumps in bacteria. Clin. Microbiol. Rev. 2006, 19, 382–402.
Omote, H.; Hiasa, M.; Matsumoto, T.; Otsuka, M.; Moriyama, Y. The MATE proteins as fundamental transporters of metabolic and xenobiotic organic cations. Trends Pharmacol. Sci. 2006, 27, 11.
Takanashi, K.; Shitan, N.; Yazaki, K. The multidrug and toxic compound extrusion (MATE) family in plants. Plant Biotechnol. 2014, 31, 417–430.
Kusakizako, T.; Miyauchi, H.; Ishitani, R.; Nureki, O. Structural biology of the multidrug and toxic compound extrusion superfamily transporters. Biochim. Biophys. Acta-Biomembr. 2020, 1862, 183154.
Ng, M.-S.; Ku, Y.-S.; Yung, W.-S.; Cheng, S.-S.; Man, C.-K.; Yang, L.; Song, S.; Chung, G.; Lam, H.-M. MATE-type proteins are responsible for isoflavone transportation and accumulation in soybean seeds. Int. J. Mol. Sci. 2021, 22, 12017.
Ku, Y.-S.; Cheng, S.-S.; Cheung, M.-Y.; Niu, Y.; Liu, A.; Chung, G.; Lam, H.-M. The poly-glutamate motif of GmMATE4 regulates its isoflavone transport activity. Membranes 2022, 12, 206.
Pérez-Díaz, R.; Ryngajllo, M.; Pérez-Díaz, J.; Peña-Cortés, H.; Casaretto, J.A.; González-Villanueva, E.; Ruiz-Lara, S. VvMATE1 and VvMATE2 encode putative proanthocyanidin transporters expressed during berry development in Vitis vinifera L. Plant Cell Rep. 2014, 33, 1147–1159.
Ku, Y.-S.; Ng, M.-S.; Cheng, S.-S.; Lo, A.W.-Y.; Xiao, Z.; Shin, T.-S.; Chung, G.; Lam, H.-M. Understanding the composition, biosynthesis, accumulation and transport of flavonoids in crops for the promotion of crops as healthy sources of flavonoids for human consumption. Nutrients 2020, 12, 1717.
Upadhyay, N.; Kar, D.; Deepak Mahajan, B.; Nanda, S.; Rahiman, R.; Panchakshari, N.; Bhagavatula, L.; Datta, S. The multitasking abilities of MATE transporters in plants. J. Exp. Bot. 2019, 70, 4643–4656.
Biała-Leonhard, W.; Zanin, L.; Gottardi, S.; de Brito Francisco, R.; Venuti, S.; Valentinuzzi, F.; Mimmo, T.; Cesco, S.; Bassin, B.; Martinoia, E.; et al. Identification of an isoflavonoid transporter required for the nodule establishment of the Rhizobium-Fabaceae symbiotic interaction. Front. Plant Sci. 2021, 12, 758213.
Gonzalez, A.; Brown, M.; Hatlestad, G.; Akhavan, N.; Smith, T.; Hembd, A.; Moore, J.; Montes, D.; Mosley, T.; Resendez, J.; et al. TTG2 controls the developmental regulation of seed coat tannins in Arabidopsis by regulating vacuolar transport steps in the proanthocyanidin pathway. Dev. Biol. 2016, 419, 54–63.
Zhang, H.; Zhao, F.; Tang, R.; Yu, Y.; Song, J.; Wang, Y.; Li, L. Two tonoplast MATE proteins function as turgor-regulating chloride channels in Arabidopsis. Proc. Natl. Acad. Sci. USA 2017, 144, E2036–E2045.
Doshi, R.; McGrath, A.P.; Piñeros, M.; Szewczyk, P.; Garza, D.M.; Kochian, L.V.; Chang, G. Functional characterization and discovery of modulators of SbMATE, the agronomically important aluminium tolerance transporter from Sorghum bicolor. Sci. Rep. 2017, 7, 17996.
Zhang, J.; Wei, J.; Li, D.; Kong, X.; Rengel, Z.; Chen, L.; Yang, Y.; Cui, X.; Chen, Q. The role of the plasma membrane H+-ATPase in plant responses to aluminum toxicity. Front. Plant Sci. 2017, 8, 1757.
Zhang, H.; Zhu, H.; Pan, Y.; Yu, Y.; Luan, S.; Li, L. A DTX/MATE-type transporter facilitates abscisic acid efflux and modulates ABA sensitivity and drought tolerance in Arabidopsis. Mol. Plant 2014, 7, 1522–1532.
Serrano, M.; Wang, B.; Aryal, B.; Garcion, C.; Abou-Mansour, E.; Heck, S.; Geisler, M.; Mauch, F.; Nawrath, C.; Métraux, J.-P. Export of salicylic acid from the chloroplast requires the multidrug and toxin extrusion-like transporter EDS5. Plant Physiol. 2013, 162, 1815–1821.
Nawrath, C.; Heck, S.; Parinthawong, N.; Métraux, J.-P. EDS5, an essential component of salicylic acid-dependent signaling for disease resistance in Arabidopsis, is a member of the MATE transporter family. Plant Cell 2002, 14, 275–286.
Morita, M.; Shitan, N.; Sawada, K.; Van Mongtagu, M.C.E.; Inzéc, D.; Rischer, H.; Goossens, A.; Oksman-caldentey, K.; Moriyama, Y.; Yazaki, K. Vacuolar transport of nicotine is mediated by a multidrug and toxic compound extrusion (MATE) transporter in Nicotiana tabacum. Proc. Natl. Acad. Sci. USA 2009, 106, 2447–2452.
Heiser, C.B. Aspects of unconscious selection and the evolution of domesticated plants. Euphytica 1988, 37, 77–81.
Ferreira, V.; Pinto-Carnide, O.; Arroyo-García, R.; Castro, I. Berry color variation in grapevine as a source of diversity. Plant Physiol. Biochem. 2018, 132, 696–707.
Ladizinsky, G. Pulse domestication before cultivation. Econ. Bot. 1987, 41, 60–65.
Tushingham, S.; Ardura, D.; Eerkens, J.W.; Palazoglu, M.; Shahbaz, S.; Fiehn, O. Hunter-gatherer tobacco smoking: Earliest evidence from the Pacific Northwest Coast of North America. J. Archaeol. Sci. 2013, 40, 1397–1407.
Cowan, M.F.; Blomstedt, C.K.; Møller, B.L.; Henry, R.J.; Gleadow, R.M. Variation in production of cyanogenic glucosides during early plant development: A comparison of wild and domesticated sorghum. Phytochemistry 2021, 184.
Ye, J.; Wang, X.; Hu, T.; Zhang, F.; Wang, B.; Li, C.; Yang, T.; Li, H.; Lu, Y.; Giovannoni, J.J.; et al. An InDel in the promoter of AI-ACTIVATED MALATE TRANSPORTER9 selected during tomato domestication determines fruit malate contents and aluminum tolerance. Plant Cell 2017, 29, 2249–2268.
Vaughan, D.A.; Balázs, E.; Heslop-Harrison, J.S. From crop domestication to super-domestication. Ann. Bot. 2007, 100, 893–901.
Yamasaki, M.; Wright, S.I.; McMullen, M.D. Genomic screening for artificial selection during domestication and improvement in maize. Ann. Bot. 2007, 100, 967–973.
Shi, J.; Lai, J. Patterns of genomic changes with crop domestication and breeding. Curr. Opin. Plant Biol. 2015, 24, 47–53.
Doebley, J.; Stec, A.; Gustus, C. teosinte branched1 and the origin of maize: Evidence for epistasis and the evolution of dominance. Genetics 1995, 141, 333–346.
Doebley, J.; Stec, A.; Hubbard, L. The evolution of apical dominance in maize. Nature 1997, 386, 485–488.
Zhang, D.; Zhang, H.; Hu, Z.; Chu, S.; Yu, K.; Lv, L.; Yang, Y.; Zhang, X.; Chen, X.; Kan, G.; et al. Artificial selection on GmOLEO1 contributes to the increase in seed oil during soybean domestication. PLoS Genet. 2019, 15, e1008267.
Zhu, B.F.; Si, L.; Wang, Z.; Zhou, Y.; Zhu, J.; Shangguan, Y.; Lu, D.; Fan, D.; Li, C.; Lin, H.; et al. Genetic control of a transition from black to straw-white seed hull in rice domestication. Plant Physiol. 2011, 155, 1301–1311.
Kumar, A.; Anju, T.; Kumar, S.; Chhapekar, S.S.; Sreedharan, S.; Singh, S.; Choi, S.R.; Ramchiary, N.; Lim, Y.P. Integrating omics and gene editing tools for rapid improvement of traditional food plants for diversified and sustainable food security. Int. J. Mol. Sci. 2021, 22, 8093.
Doebley, J.F.; Gaut, B.S.; Smith, B.D. The molecular genetics of crop domestication. Cell 2006, 127, 1309–1321.
Dehaan, L.R.; Van Tassel, D.L.; Anderson, J.A.; Asselin, S.R.; Barnes, R.; Baute, G.J.; Cattani, D.J.; Culman, S.W.; Dorn, K.M.; Hulke, B.S.; et al. A pipeline strategy for grain crop domestication. Crop Sci. 2016, 56, 917–930.
Ku, Y.-S.; Contador, C.A.; Ming-Sin, N.; Yu, J.; Chung, G.; Lam, H.-M. The effects of domestication on secondary metabolite composition in legumes. Front. Genet. 2020, 11, 581357.
Alseekh, S.; Scossa, F.; Wen, W.; Luo, J.; Yan, J.; Beleggia, R.; Klee, H.J.; Huang, S.; Papa, R.; Fernie, A.R. Domestication of crop metabolomes: Desired and unintended consequences. Trends Plant Sci. 2021, 26, 650–661.
Brown, A.H.D. Variation under domestication in plants: 1859 and today. Philos. Trans. R. Soc. B Biol. Sci. 2010, 365, 2523–2530.
Xu, R.; Sun, C. What happened during domestication of wild to cultivated rice. Crop J. 2021, 9, 564–576.
Stetter, M.G.; Vidal-Villarejo, M.; Schmid, K.J. Parallel seed color adaptation during multiple domestication attempts of an ancient new world grain. Mol. Biol. Evol. 2019, 37, 1407–1419.
Bruno, M.C. Quinoa: Origins and development. In Encyclopeida of Global Archaeology; Smith, C., Ed.; Springer: New York, NY, USA, 2014; ISBN 9781441904652.
Tanaka, Y.; Sasaki, N.; Ohmiya, A. Biosynthesis of plant pigments: Anthocyanins, betalains and carotenoids. Plant J. 2008, 54, 733–749.
Pandey, R.N.; Pawar, S.E.; Chintalwar, G.J.; Bhatia, C.R. Seed coat and hypocotyl pigments in greengram and blackgram. Proc. Indian Acad. Sci. (Plant Sci.) 1989, 99, 301–306.
Elessawy, F.M.; Bazghaleh, N.; Vandenberg, A.; Purves, R.W. Polyphenol profile comparisons of seed coats of five pulse crops using a semi-quantitative liquid chromatography-mass spectrometric method. Phytochem. Anal. 2020, 31, 458–471.
Debeaujon, I.; Peeters, A.J.M.; Léon-Kloosterziel, K.M.; Koornneef, M. The TRANSPARENT TESTA12 gene of Arabidopsis encodes a multidrug secondary transporter-like protein required for flavonoid sequestration in vacuoles of the seed coat endothelium. Plant Cell 2001, 13, 853–872.
Marinova, K.; Pourcel, L.; Weder, B.; Schwarz, M.; Barron, D.; Routaboul, J.-M.; Debeaujon, I.; Klein, M. The Arabidopsis MATE transporter TT12 acts as a vacuolar flavonoid/H+- antiporter active in proanthocyanidin-accumulating cells of the seed coat. Plant Cell 2007, 19, 2023–2038.
Stone, M. Taming the wild carrot. Bioscience 2016, 66, 912.
Iorizzo, M.; Senalik, D.A.; Ellison, S.L.; Grzebelus, D.; Cavagnaro, P.F.; Allender, C.; Brunet, J.; Spooner, D.M.; Deynze, A.V.; Simon, P.W. Genetic structure and domestication of carrot (Daucus varota subsp. sativus) (Apiaceae). Am. J. Bot. 2013, 100, 930–938.
Pierre, M.D.S.; Bayer, R.J. The impact of domestication on the genetic variability in the orange carrot, cultivated Daucus carota ssp. sativus and the genetic homogeneity of various cultivars. Theor. Appl. Genet. 1991, 82, 249–253.
Fournier-Level, A.; Lacombe, T.; Le Cunff, L.; Boursiquot, J.-M.; This, P. Evolution of the VvMybA gene family, the major determinant of berry colour in cultivated grapevine (Vitis vinifera L.). Heredity 2010, 104, 351–362.
Sun, T.; Xu, L.; Sun, H.; Yue, Q.; Zhai, H.; Yao, Y. VvVHP1;2 is transcriptionally activated by VvMYBA1 and promotes anthocyanin accumulation of grape berry skins via glucose signal. Front. Plant Sci. 2017, 8, 1811.
Bewley, J.D. Seed germination and dormancy. Plant Cell 1997, 9, 1055–1066.
Rodríguez-Gacio, M.D.C.; Matilla-Vázquez, M.A.; Matilla, A.J. Seed dormancy and ABA signaling: The breakthrough goes on. Plant Signal. Behav. 2009, 4, 1035–1048.
Skubacz, A.; Daszkowska-Golec, A. Seed dormancy: The complex process regulated by abscisic acid, gibberellins, and other phytohormones that makes seed germination work. In Phytohormones—Signaling Mechanisms and Crosstalk in Plant Development and Stress Responses; El-Esawi, M.A., Ed.; Intech Open: London, UK, 2017.
Shu, K.; Liu, X.-D.; Xie, Q.; He, Z.-H. Two faces of one seed: Hormonal regulation of dormancy and germination. Mol. Plant 2016, 9, 34–45.
Kanno, Y.; Jikumaru, Y.; Hanada, A.; Nambara, E.; Abrams, S.R.; Kamiya, Y.; Seo, M. Comprehensive hormone profiling in developing Arabidopsis seeds: Examination of the site of ABA biosynthesis, ABA transport and hormone interactions. Plant Cell Physiol. 2010, 51, 1988–2001.
Lee, K.P.; Piskurewicz, U.; Turečková, V.; Strnad, M.; Lopez-Molina, L. A seed coat bedding assay shows that RGL2-dependent release of abscisic acid by the endosperm controls embryo growth in Arabidopsis dormant seeds. Proc. Natl. Acad. Sci. USA 2010, 107, 19108–19113.
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.
Park, J.; Lee, Y.; Martinoia, E.; Geisler, M. Plant hormone transporters: What we know and what we would like to know. BMC Biol. 2017, 15, 93.
Yue, X.; Liang, J.; Gu, F.; Du, D.; Chen, F. Berberine activates bitter taste responses of enteroendocrine STC-1 cells. Mol. Cell. Biochem. 2018, 447, 21–32.
Shitan, N. Secondary metabolites in plants: Transport and self-tolerance mechanisms. Biosci. Biotechnol. Biochem. 2016, 80, 1283–1293.
Takanashi, K.; Yamada, Y.; Sasaki, T.; Yamamoto, Y.; Sato, F.; Yazaki, K. A multidrug and toxic compound extrusion transporter mediates berberine accumulation into vacuoles in Coptis japonica. Phytochemistry 2017, 138, 76–82.
Gao, Y.; Wang, F.; Song, Y.; Liu, H. The status of and trends in the pharmacology of berberine: A bibliometric review . Chin. Med. 2020, 15, 7.
Gleadow, R.M.; Møller, B.L. Cyanogenic glycosides: Synthesis, physiology, and phenotypic plasticity. Annu. Rev. Plant Biol. 2014, 65, 155–185.
Dillon, S.L.; Shapter, F.M.; Henry, R.J.; Cordeiro, G.; Izquierdo, L.; Lee, L.S. Domestication to crop improvement: Genetic resources for Sorghum and Saccharum (Andropogoneae). Ann. Bot. 2007, 100, 975–989.
Gleadow, R.M.; Møldrup, M.E.; O’Donnell, N.H.; Stuart, P.N. Drying and processing protocols affect the quantification of cyanogenic glucosides in forage sorghum. J. Sci. Food Agric. 2012, 92, 2234–2238.
Møller, B.L. Functional diversifications of cyanogenic glucosides. Curr. Opin. Plant Biol. 2010, 13, 337–346.
Bjarnholt, N.; Neilson, E.H.J.; Crocoll, C.; Jørgensen, K.; Motawia, M.S.; Olsen, C.E.; Dixon, D.P.; Edwards, R.; Møller, B.L. Glutathione transferases catalyze recycling of auto-toxic cyanogenic glucosides in sorghum. Plant J. 2018, 94, 1109–1125.
Darbani, B.; Motawia, M.S.; Olsen, C.E.; Nour-Eldin, H.H.; Møller, B.L.; Rook, F. The biosynthetic gene cluster for the cyanogenic glucoside dhurrin in Sorghum bicolor contains its co-expressed vacuolar MATE transporter. Sci. Rep. 2016, 6, 37079.
Duke, D.; Wohlgemuth, E.; Adams, K.R.; Armstrong-Ingram, A.; Rice, S.K.; Young, D.C. Earliest evidence for human use of tobacco in the Pleistocene Americas. Nat. Hum. Behav. 2021, 6, 183–192.
Shitan, N.; Minami, S.; Morita, M.; Hayashida, M.; Ito, S.; Takanashi, K.; Omote, H.; Moriyama, Y.; Sugiyama, A.; Goossens, A.; et al. Involvement of the leaf-specific multidrug and toxic compound extrusion (MATE) transporter Nt-JAT2 in vacuolar sequestration of nicotine in Nicotiana tabacum. PLoS One 2014, 9, e108789.
Shoji, T.; Inai, K.; Yazaki, Y.; Sato, Y.; Takase, H.; Shitan, N.; Yazaki, K.; Goto, Y.; Toyooka, K.; Matsuoka, K.; et al. Multidrug and toxic compound extrusion-type transporters implicated in vacuolar sequestration of nicotine in tobacco roots. Plant Physiol. 2009, 149, 708–718.
Wang, B.; Lewis, R.S.; Shi, J.; Song, Z.; Gao, Y.; Li, W.; Chen, H.; Qu, R. Genetic factors for enhancement of nicotine levels in cultivated tobacco. Sci. Rep. 2015, 5, 17360.
Liu, H.; Kotova, T.I.; Timko, M.P. Increased leaf nicotine content by targeting transcription factor gene expression in commercial flue-cured tobacco (Nicotiana tabacum L.). Genes 2019, 10, 930.
Zhang, H.-B.; Bokowiec, M.T.; Rushton, P.J.; Han, S.-C.; Timko, M.P. Tobacco transcription factors NtMYC2a and NtMYC2b form nuclear complexes with the NtJAZ1 repressor and regulate multiple jasmonate-inducible steps in nicotine biosynthesis. Mol. Plant 2012, 5, 73–84.

© Text is available under the terms and conditions of the Creative Commons Attribution (CC BY) license; additional terms may apply. By using this site, you agree to the Terms and Conditions and Privacy Policy.

Upload a video for this entry

Information

Subjects: Agriculture, Dairy & Animal Science

Contributors MDPI registered users' name will be linked to their SciProfiles pages. To register with us, please refer to https://encyclopedia.pub/register :

View Times: 590

Update Date: 05 May 2022

Table of Contents

Video Upload Options

Confirm