Aluminum stress signaling, response, and adaptive mechanisms in plants

Figures & data

Figure 1. Proposed model for the regulation of malate and citrate secretion by STOP1 in response to Al stress and the proposed signaling pathway of Al-activated root malate and citrate exudation based on recent research on Arabidopsis.^{6,18,73,94,95} In response to Al stress, Al³⁺ signals can be perceived by the plant and trigger the accumulation of STOP1 in the cell. As a transcription factor, STOP1 upregulates the expression of RAE1, ALMT1, and MATE. RAE1 reduces the amount of STOP1 by promoting the ubiquitination (Ub) and degradation of STOP1.^6,18,95 Al-activated excretion of malate and citrate occurs through the PM localized transporters of ALMT1 and MATE, respectively. The secretion of OAs plays a critical role in plant Al tolerance through the chelation of external Al.

Table 1. Related genes responsible for Al-activated secretion of OAs and plant Al-resistance

Gene	GenBank accession	Gene type	The subcellular location	Species	Gene expression patterns	References
AtMATE	At1g51340	Citrate transporter	Plasma membrane	Arabidopsis thaliana	Al-induced up-regulation	^Citation6,Citation73
ZmMATE1	Zm00001d035115	Citrate transporter		Zea mays (Maize)	Al-induced up-regulation	^Citation25,Citation78
SbMATE	EF611342	Citrate transporter	Plasma membrane	Sorghum bicolor (Sorghum)	Al-induced up-regulation	^Citation96
HvAACT1/HvMATE1	AB331641	Citrate transporter	Plasma membrane	Hordeum vulgare (Barley)		^Citation97
TaMATE1	BE605049	Citrate transporter, belonging to the multidrug and toxin efflux (MATE) gene family		Triticum aestivum (Wheat)		^Citation98
FeMATE1	comp57549_c0	Multi-drug and toxic compound extrusion	Plasma membrane	Fagopyrum esculentum (Buckwheat)	Al-induced up-regulation	^Citation99,Citation100
FeMATE2	comp55339_c0	Multi-drug and toxic compound extrusion	Trans-Golgi and Golgi	Fagopyrum esculentum (Buckwheat)	Al-induced up-regulation and leaves	^Citation99,Citation100
OsFRDL4	Os01g0919100	Citrate transporter, belongs to the multidrug and toxic compound extrusion (MATE) family	Plasma membrane	Oryza sativa (Rice)	Al-induced up-regulation	^Citation90
AtALMT1	At1g08430	Al-activated malate transporter 1	Plasma membrane	Arabidopsis thaliana	Al-induced up-regulation	^Citation18,Citation73,Citation77
TaALMT1	AB081803	Al-activated efflux of malate	Plasma membrane	Triticum aestivum (Wheat)		^Citation85
VHA-a2	At2g21410	The vacuolar H1-ATPase, vacuolar H1-translocating adenosine triphosphatase (H1-ATPase) subunit a2		Arabidopsis thaliana	Al-induced down- regulation	^Citation18
VHA-a3	At4g39080	The vacuolar H1-ATPase, vacuolar H1-translocating adenosine triphosphatase (H1-ATPase) subunit a3		Arabidopsis thaliana	Al-induced down- regulation	^Citation18
ESD4	At4g15880	The small ubiquitin-like modifier (SUMO) protease	Nuclear rim	Arabidopsis thaliana		^Citation94,Citation101,Citation102
HPR1	At5g09860	Hyperrecombination protein 1 (HPR1), a subunit of the THO/TREX complex	Nucleus	Arabidopsis thaliana		^Citation95
RAE1	At5g01720	The F-box protein Regulation of AtALMT1 Expression 1 (RAE1)	Nucleus	Arabidopsis thaliana	Al-induced up-regulation	^Citation6,Citation103
RAH1	At5g27920	RAE1 homolog 1	Nucleus	Arabidopsis thaliana	Al-induced up-regulation	^Citation103
STOP1	At1g34370	The C2H2-type zinc finger transcription factor sensitive to proton rhizotoxicity 1		Arabidopsis thaliana	STOP1 transcription is not affected by Al stress, Al stress triggers STOP1 protein accumulation.	^Citation6
STAR1	AB253626	a bacterial-type ATP binding cassette (ABC) transporter, sensitive to Al rhizotoxicity1	The vesicle membrane	Oryza sativa (Rice)	Al-induced up-regulation	^Citation104
STAR2	AB379845	a bacterial-type ATP binding cassette (ABC) transporter	The vesicle membrane	Oryza sativa (Rice)	Al-induced up-regulation	^Citation104
ALS1	At5g39040	The ATP-binding cassette (ABC) transporter, aluminum-sensitive 1	Vacuolar membrane	Arabidopsis thaliana		^Citation105
ALS3	At2g37330	The ATP-binding cassette (ABC) transporter-like protein	Plasma membrane	Arabidopsis thaliana		^Citation6,Citation93

Table 2. Hormone signaling-related genes in plant response to Al stress

Gene	GenBank accession	Gene type	The subcellular location	Species	Gene expression patterns	References
ACS2	AT1G01480	Ethylene synthesis genes		Arabidopsis thaliana	Al-induced up-regulation	^Citation19
ACS4	AT2G22810	Ethylene synthesis genes		Arabidopsis thaliana	Al-induced up-regulation	^Citation19
ACS6	AT4G11280	Ethylene synthesis genes		Arabidopsis thaliana	Al-induced up-regulation	^Citation19
ACO1	AT2G19590	Ethylene synthesis genes		Arabidopsis thaliana	Al-induced up-regulation	^Citation19
ACO2	AT1G62380	Ethylene synthesis genes		Arabidopsis thaliana	Al-induced up-regulation	^Citation19
EBS		Ethylene reporter, a synthetic EIN3-responsive promoter		Arabidopsis thaliana	Al-induced up-regulation	^Citation19
EIL1	AT2G27050	Ethylene signaling, transcription factors		Arabidopsis thaliana	Al-induced up-regulation	^Citation20
EIN3	AT3G20770	Ethylene signaling, ethylene-insensitive 3 (EIN3)		Arabidopsis thaliana	Al-induced up-regulation	^Citation20
DR5		Auxin-responsive marker		Zea mays (Maize)	Al-induced down-regulation	^Citation25
DR5		Auxin-responsive marker		Arabidopsis thaliana	Al-induced up-regulation	^Citation19
TAA1	AT1G70560	Auxin biosynthesis, Trp aminotransferase		Arabidopsis thaliana	Al-induced up-regulation	^Citation8
YUC3	AT1G04610	Auxin biosynthesis		Arabidopsis thaliana	Al-induced up-regulation	^Citation20
YUC5	AT5G43890	Auxin biosynthesis		Arabidopsis thaliana	Al-induced up-regulation	^Citation20
YUC7	AT2G33230	Auxin biosynthesis		Arabidopsis thaliana	Al-induced up-regulation	^Citation20
YUC8	AT4G28720	Auxin biosynthesis		Arabidopsis thaliana	Al-induced up-regulation	^Citation20
YUC9	AT1G04180	Auxin biosynthesis		Arabidopsis thaliana	Al-induced up-regulation	^Citation20
PIN1	AT1G73590	Auxin efflux carriers	Plasma membrane	Arabidopsis thaliana	Al-induced ectopically up-regulated	^Citation108
PIN2	AT5G57090	Auxin efflux carriers	Plasma membrane	Arabidopsis thaliana	Al-induced up-regulation	^Citation19,Citation108
OsPIN2	Os06g44970	Auxin efflux carriers	Plasma membrane	Oryza sativa (Rice)	Al-induced up-regulation	^Citation109
PIN3	AT1G70940	Auxin efflux carriers	Plasma membrane	Arabidopsis thaliana	Al-induced ectopically up-regulated	^Citation108
PIN4	AT2G01420	Auxin efflux carriers	Plasma membrane	Arabidopsis thaliana	Al-induced ectopically up-regulated	^Citation108
PIN7	AT1G23080	Auxin efflux carriers	Plasma membrane	Arabidopsis thaliana	Al-induced ectopically up-regulated	^Citation108
AUX1	AT2G38120	Auxin influx carriers	Plasma membrane	Arabidopsis thaliana	Al-induced ectopically up-regulated	^Citation19,Citation108
LAX1	AT5G01240	Auxin influx carriers	Plasma membrane	Arabidopsis thaliana	Al-induced ectopically up-regulated	^Citation108
LAX2	AT2G21050	Auxin influx carriers	Plasma membrane	Arabidopsis thaliana	Al-induced ectopically up-regulated	^Citation108
ZmPGP1	GRMZM2G315375	Auxin efflux carrier P-glycoprotein		Zea mays (Maize)	Al-induced up-regulation	^Citation25
ARF7	AT5G20730	Auxin response factors		Arabidopsis thaliana	Al-induced up-regulation	^Citation110
ARF10	AT2G28350	Auxin response factors (ARFs), ARF10 is important in the regulation of cell wall modification–related genes		Arabidopsis thaliana		^Citation8
ARF16	AT4G30080	auxin response factors (ARFs), ARF16 is important in the regulation of cell wall modification–related genes		Arabidopsis thaliana		^Citation8
ZmIAA2	Zm00001d033976	Auxin-responsive genes		Zea mays (Maize)	Al-induced down- regulation	^Citation25
ZmIAA10	Zm00001d041416	Auxin-responsive genes		Zea mays (Maize)	Al-induced down- regulation	^Citation25
ZmIAA21	Zm00001d013302	Auxin-responsive genes		Zea mays (Maize)	Al-induced down- regulation	^Citation25
ZmGH3	Zm00001d011377	Auxin-responsive genes		Zea mays (Maize)	Al-induced down- regulation	^Citation25
ARR3	AT1G59940	CK-induced genes		Arabidopsis thaliana	Al-induced up-regulation	^Citation110
ARR4	AT1G10470	CK-induced genes		Arabidopsis thaliana	Al-induced up-regulation	^Citation110
TCSn		CK signaling, Two Component Signaling Sensor new (TCSn)		Arabidopsis thaliana	Al-induced up-regulation	^Citation110
IPT1	AT1G68460	Cytokinin biosynthesis, adenosine phosphate isopentenyl-transferases		Arabidopsis thaliana	Al-induced up-regulation	^Citation110
IPT3	AT3G63110	Cytokinin biosynthesis		Arabidopsis thaliana	Al-induced up-regulation	^Citation110
IPT5	AT5G19040	Cytokinin biosynthesis		Arabidopsis thaliana	Al-induced up-regulation	^Citation110
IPT7	AT3G23630	Cytokinin biosynthesis		Arabidopsis thaliana	Al-induced up-regulation	^Citation110
PIF4	AT2G43010	The basic helix–loop–helix transcription factors, Phytochrome-interacting factor 4 (PIF4)		Arabidopsis thaliana	Al-induced up-regulation	^Citation20
COI1	AT2G39940	Jasmonate (JA) receptor, Coronatine Insensitive 1		Arabidopsis thaliana	Al-induced up-regulation	^Citation111
MYC2	AT1G32640	JA signaling regulator		Arabidopsis thaliana	Al-induced up-regulation	^Citation111
AOS	AT5G42650	JA biosynthesis related genes		Arabidopsis thaliana	Al-induced up-regulation	^Citation111
AOC3	AT3G25780	JA biosynthesis related genes, Allene Oxide Cyclase 3		Arabidopsis thaliana	Al-induced up-regulation	^Citation111
OPR3	At2g06050	JA biosynthesis related genes, Oxophytodienoate-reductase 3		Arabidopsis thaliana	Al-induced up-regulation	^Citation111

Figure 2. Schematic representation of ethylene- and auxin-mediated regulation of root growth inhibition in response to Al stress. The proposed hormone signaling pathway under Al stress was based on recent research on plants.^{8,19,20,87,108,110,111,114,115} The root tip is considered the main site that identifies Al toxicity. The transition zone (TZ) between the meristem and the elongation zone of the root apex is the most sensitive area for plants to perceive Al stress. Al stress induces auxin response in the root TZ, which is dependent on the ethylene signaling pathway. Al³⁺ was found to upregulate the expression of ACSs and ACOs and promote ethylene biosynthesis.¹⁹ Ethylene promotes local auxin accumulation through TAA1- and YUCs-mediated local auxin biosynthesis.^8,20,110 In addition, ethylene promotes local auxin accumulation through AUX1- and PIN2-mediated polar auxin transport, resulting in root growth inhibition.^19,108 ARF-mediated auxin signaling controls the Al-induced inhibition of root growth by regulating IPT-dependent cytokinin biosynthesis and cell wall modification-related genes.^8,110,111

Zhang Y, Zhang J, Guo J, Zhou F, Singh S, Xu X, Xie Q, Yang Z, Huang CF. F-box protein RAE1 regulates the stability of the aluminum-resistance transcription factor STOP1 in Arabidopsis. Proc Natl Acad Sci U S A. 2019;116(1):319–327. doi:10.1073/pnas.1814426116.

 PubMed Web of Science ®Google Scholar

Zhang F, Yan X, Han X, Tang R, Chu M, Yang Y, Yang YH, Zhao F, Fu A, Luan S, et al. A defective vacuolar proton pump enhances aluminum tolerance by reducing vacuole sequestration of organic acids. Plant Physiol. 2019;181(2):743–761. doi:10.1104/pp.19.00626.

 PubMed Web of Science ®Google Scholar

Liu J, Magalhaes JV, Shaff J, Kochian LV. Aluminum-activated citrate and malate transporters from the MATE and ALMT families function independently to confer Arabidopsis aluminum tolerance. Plant J. 2009;57(3):389–399. doi:10.1111/j.1365-313X.2008.03696.x.

 PubMed Web of Science ®Google Scholar

Fang Q, Zhang J, Zhang Y, Fan N, van den Burg HA, Huang CF. Regulation of aluminum resistance in Arabidopsis involves the SUMOylation of the zinc finger transcription factor STOP1. Plant Cell. 2020;32(12):3921–3938. doi:10.1105/tpc.20.00687.

 PubMed Web of Science ®Google Scholar

Guo J, Zhang Y, Gao H, Li S, Wang ZY, Huang CF. Mutation of HPR1 encoding a component of the THO/TREX complex reduces STOP1 accumulation and aluminium resistance in Arabidopsis thaliana. New Phytol. 2020;228(1):179–193. doi:10.1111/nph.16658.

 PubMed Web of Science ®Google Scholar

Zhang M, Lu X, Li C, Zhang B, Zhang C, Zhang XS, Ding Z. Auxin efflux carrier ZmPGP1 mediates root growth inhibition under aluminum stress. Plant Physiol. 2018;177(2):819–832. doi:10.1104/pp.17.01379.

 PubMed Web of Science ®Google Scholar

Maron LG, Piñeros MA, Guimarães CT, Magalhaes JV, Pleiman JK, Mao C, Shaff J, Belicuas SN, Kochian LV. Two functionally distinct members of the MATE (multi-drug and toxic compound extrusion) family of transporters potentially underlie two major aluminum tolerance QTLs in maize. Plant J. 2010;61(5):728–740. doi:10.1111/j.1365-313X.2009.04103.x.

 PubMed Web of Science ®Google Scholar

Magalhaes JV, Liu J, Guimarães CT, Lana UG, Alves VM, Wang YH, Schaffert RE, Hoekenga OA, Piñeros MA, Shaff JE, et al. A gene in the multidrug and toxic compound extrusion (MATE) family confers aluminum tolerance in sorghum. Nat Genet. 2007;39(9):1156–1161. doi:10.1038/ng2074.

 PubMed Web of Science ®Google Scholar

Furukawa J, Yamaji N, Wang H, Mitani N, Murata Y, Sato K, Katsuhara M, Takeda K, Ma JF. An aluminum-activated citrate transporter in barley. Plant Cell Physiol. 2007;48(8):1081–1091. doi:10.1093/pcp/pcm091.

 PubMed Web of Science ®Google Scholar

Ryan PR, Raman H, Gupta S, Horst WJ, Delhaize E. A second mechanism for aluminum resistance in wheat relies on the constitutive efflux of citrate from roots. Plant Physiol. 2009;149(1):340–351. doi:10.1104/pp.108.129155.

 PubMed Web of Science ®Google Scholar

Yokosho K, Yamaji N, Ma JF. Global transcriptome analysis of Al-induced genes in an Al-accumulating species, common buckwheat (Fagopyrum esculentum Moench). Plant Cell Physiol. 2014;55(12):2077–2091. doi:10.1093/pcp/pcu135.

 PubMed Web of Science ®Google Scholar

Lei GJ, Yokosho K, Yamaji N, Ma JF. Two MATE transporters with different subcellular localization are involved in Al tolerance in buckwheat. Plant Cell Physiol. 2017;58(12):2179–2189. doi:10.1093/pcp/pcx152.

 PubMed Web of Science ®Google Scholar

Yokosho K, Yamaji N, Ma JF. An Al-inducible MATE gene is involved in external detoxification of Al in rice. Plant J. 2011;68(6):1061–1069. doi:10.1111/j.1365-313X.2011.04757.x.

 PubMed Web of Science ®Google Scholar

Hoekenga OA, Maron LG, Piñeros MA, Cançado GM, Shaff J, Kobayashi Y, Ryan PR, Dong B, Delhaize E, Sasaki T, et al. AtALMT1, which encodes a malate transporter, is identified as one of several genes critical for aluminum tolerance in Arabidopsis. Proc Natl Acad Sci U S A. 2006;103(25):9738–9743. doi:10.1073/pnas.0602868103.

 PubMed Web of Science ®Google Scholar

Sasaki T, Yamamoto Y, Ezaki B, Katsuhara M, Ahn SJ, Ryan PR, Delhaize E, Matsumoto H. A wheat gene encoding an aluminum-activated malate transporter. Plant J. 2004;37(5):645–653. doi:10.1111/j.1365-313X.2003.01991.x.

 PubMed Web of Science ®Google Scholar

Murtas G, Reeves PH, Fu YF, Bancroft I, Dean C, Coupland G. A nuclear protease required for flowering-time regulation in Arabidopsis reduces the abundance of SMALL UBIQUITIN-RELATED MODIFIER conjugates. Plant Cell. 2003:15, 2308–2319.

 Google Scholar

Xu XM, Rose A, Muthuswamy S, Jeong SY, Venkatakrishnan S, Zhao Q, Meier I. NUCLEAR PORE ANCHOR, the Arabidopsis Homolog of Tpr/Mlp1/Mlp2/Megator, Is Involved in mRNA Export and SUMO Homeostasis and Affects Diverse Aspects of Plant Development. Plant Cell. 2007;19(5):1537–1548. doi:10.1105/tpc.106.049239.

 PubMed Web of Science ®Google Scholar

Fang Q, Zhou F, Zhang Y, Singh S, Huang CF. Degradation of STOP1 mediated by the F-box proteins RAH1 and RAE1 balances aluminum resistance and plant growth in Arabidopsis thaliana. Plant J. 2021;106(2):493–506. doi:10.1111/tpj.15181.

 PubMed Web of Science ®Google Scholar

Huang CF, Yamaji N, Mitani N, Yano M, Nagamura Y, Ma JF. A bacterial-type ABC transporter is involved in aluminum tolerance in rice. Plant Cell. 2009;21(2):655–667. doi:10.1105/tpc.108.064543.

 PubMed Web of Science ®Google Scholar

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

 Google Scholar

Larsen PB, Geisler MJ, Jones CA, Williams KM, Cancel JD. ALS3 encodes a phloem-localized ABC transporter-like protein that is required for aluminum tolerance in Arabidopsis. Plant J. 2005;41(3):353–363. doi:10.1111/j.1365-313X.2004.02306.x.

 PubMed Web of Science ®Google Scholar

Sun P, Tian QY, Chen J, Zhang WH. Aluminium-induced inhibition of root elongation in Arabidopsis is mediated by ethylene and auxin. J Exp Bot. 2010;61(2):347–356. doi:10.1093/jxb/erp306.

 PubMed Web of Science ®Google Scholar

Liu G, Gao S, Tian H, Wu W, Robert HS, Ding Z. Local transcriptional control of YUCCA regulates auxin promoted root-growth inhibition in response to aluminium stress in Arabidopsis. PLoS Genet. 2016;12:e1006360. doi:10.1371/journal.pgen.1006360.

 PubMed Web of Science ®Google Scholar

Yang ZB, Geng X, He C, Zhang F, Wang R, Horst WJ, Ding Z. TAA1-Regulated Local Auxin Biosynthesis in the Root-Apex Transition Zone Mediates the Aluminum-Induced Inhibition of Root Growth in Arabidopsis. Plant Cell. 2014;26(7):2889–2904. doi:10.1105/tpc.114.127993.

 PubMed Web of Science ®Google Scholar

Li C, Liu G, Geng X, He C, Quan T, Hayashi KI, De Smet I, Robert HS, Ding Z, Yang ZB. Local regulation of auxin transport in root-apex transition zone mediates aluminium-induced Arabidopsis root-growth inhibition. Plant J. 2021;108(1):55–66. doi:10.1111/tpj.15424.

 PubMed Web of Science ®Google Scholar

Wu D, Shen H, Yokawa K, Baluška F. Alleviation of aluminium-induced cell rigidity by overexpression of OsPIN2 in rice roots. J Exp Bot. 2014;65(18):5305–5315. doi:10.1093/jxb/eru292.

 PubMed Web of Science ®Google Scholar

Yang ZB, Liu G, Liu J, Zhang B, Meng W, Müller B, Hayashi KI, Zhang X, Zhao Z, De Smet I, et al. Synergistic action of auxin and cytokinin mediates aluminum-induced root growth inhibition in Arabidopsis. EMBO Rep. 2017;18(7):1213–1230. doi:10.15252/embr.201643806.

 PubMed Web of Science ®Google Scholar

Yang ZB, He C, Ma Y, Herde M, Ding Z. Jasmonic acid enhances Al-induced root growth inhibition. Plant Physiol. 2017;173(2):1420–1433. doi:10.1104/pp.16.01756.

 PubMed Web of Science ®Google Scholar

Chen W, Tang L, Wang J, Zhu H, Jin J, Yang J, Fan W. Research advances in the mutual mechanisms regulating response of plant roots to phosphate deficiency and aluminum toxicity. Int J Mol Sci. 2022;23(3):1137. doi:10.3390/ijms23031137.

 PubMed Web of Science ®Google Scholar

Li L, Verstraeten I, Roosjen M, Takahashi K, Rodriguez L, Merrin J, Chen J, Shabala L, Smet W, Ren H, et al. Cell surface and intracellular auxin signalling for H+ fluxes in root growth. Nature. 2021:599, 273–277.

 Google Scholar

Bai B, Bian H, Zeng Z, Hou N, Shi B, Wang J, Zhu M, Han N. miR393-mediated auxin signaling regulation is involved in root elongation inhibition in response to toxic aluminum stress in barley. Plant Cell Physiol. 2017;58(3):426–439. doi:10.1093/pcp/pcw211.

 PubMed Web of Science ®Google Scholar