TaNRAMP3 is essential for manganese transport in Triticum aestivum

Zhangqing Wang, Yanting Zhang, Chenyu Cao, Jiaming Liu, Yuan Deng, Zhenqian Zhang, Cun Wang

Stress Biology ›› 2023, Vol. 3 ›› Issue (1) : 41. DOI: 10.1007/s44154-023-00120-2
Original Paper

TaNRAMP3 is essential for manganese transport in Triticum aestivum

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Abstract

Manganese (Mn) is an essential trace element for almost all living organisms. In plants, Mn deficiency, which is occurs in calcareous soils or alkaline soils, severely limiting crop yields. However, the potential mechanism of Mn transport in Triticum aestivum is still obscure. Here, we found that TaNRAMP3, a member of the naturally resistant macrophage protein (NRAMP) family in Triticum aestivum, is located in the plasma membrane of protoplasts and functions as an influx transporter for Mn in yeast (Δsmf1). The expression of TaNRAMP3 was induced under Mn-deficiency conditions. Furthermore, TaNRAMP3-RNAi plants exhibited a sensitive phenotype, while transgenic plants overexpressing TaNRAMP3 showed a tolerant phenotype. In addition, TaNRAMP3 rescued the sensitive phenotype of Arabidopsis nramp1 mutant under Mn deficiency condition. In summary, our study reveals the key role of TaNRAMP3 in Mn transport in Triticum aestivum, allowing it to adapt to Mn-deficiency stress. These findings provide new insights for the cultivation of Mn-deficiency tolerant wheat varieties.

Keywords

Manganese / Triticum aestivum / TaNRAMP3 / Transporter

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Zhangqing Wang, Yanting Zhang, Chenyu Cao, Jiaming Liu, Yuan Deng, Zhenqian Zhang, Cun Wang. TaNRAMP3 is essential for manganese transport in Triticum aestivum. Stress Biology, 2023, 3(1): 41 https://doi.org/10.1007/s44154-023-00120-2

References

[1]
Alejandro S, Cailliatte R, Alcon C, Dirick L, Domergue F, Correia D, Castaings L, Briat JF, Mari S, Curie C (2017) Intracellular distribution of manganese by the Trans-Golgi network transporter NRAMP2 is critical for photosynthesis and cellular redox homeostasis. Plant Cell 29:3068–3084. https://doi.org/10.1105/tpc.17.00578
[2]
Alejandro S, Höller S, Meier B, Peiter E (2020) Manganese in plants: from acquisition to subcellular allocation. Front Plant Sci 11:300. https://doi.org/10.3389/fpls.2020.00300
[3]
Alscher RG, Erturk N, Heath LS (2002) Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. J Exp Bot 53:1331–1341. https://doi.org/10.1093/jexbot/53.372.1331
[4]
Andresen E, Peiter E, Küpper H (2018) Trace metal metabolism in plants. J Exp Bot 69:909–954. https://doi.org/10.1093/jxb/erx465
[5]
Cailliatte R, Lapeyre B, Briat JF, Mari S, Curie C (2009) The NRAMP6 metal transporter contributes to cadmium toxicity. Biochem J 422:217–228. https://doi.org/10.1042/bj20090655
[6]
Cailliatte R, Schikora A, Briat JF, Mari S, Curie C (2010) High-affinity manganese uptake by the metal transporter NRAMP1 is essential for Arabidopsis growth in low manganese conditions. Plant Cell 22:904–917. https://doi.org/10.1105/tpc.109.073023
[7]
Castaings L, Caquot A, Loubet S, Curie C (2016) The high-affinity metal transporters NRAMP1 and IRT1 team up to take up iron under sufficient metal provision. Sci Rep 6:37222. https://doi.org/10.1038/srep37222
[8]
Delhaize E, Gruber BD, Pittman JK, White RG, Leung H, Miao Y, Jiang L, Ryan PR, Richardson AE (2007) A role for the AtMTP11 gene of Arabidopsis in manganese transport and tolerance. Plant J 51:198–210. https://doi.org/10.1111/j.1365-313x.2007.03138.x
[9]
Eisenhut M, Hoecker N, Schmidt SB, Basgaran RM, Flachbart S, Jahns P, Eser T, Geimer S, Husted S, Weber APM, Leister D, Schneider A (2018) The plastid envelope CHLOROPLAST MANGANESE TRANSPORTER1 is essential for manganese homeostasis in Arabidopsis. Mol Plant 11:955–969. https://doi.org/10.1016/j.molp.2018.04.008
[10]
Eroglu S, Meier B, von Wirén N, Peiter E (2016) The vacuolar manganese transporter MTP8 determines tolerance to iron deficiency-induced chlorosis in Arabidopsis. Plant Physiol 170:1030–1045. https://doi.org/10.1104/pp.15.01194
[11]
Fu D, Zhang Z, Wallrad L, Wang Z, Höller S, Ju C, Schmitz-Thom I, Huang P, Wang L, Peiter E, Kudla J, Wang C (2022) Ca2+-dependent phosphorylation of NRAMP1 by CPK21 and CPK23 facilitates manganese uptake and homeostasis in Arabidopsis. Proc Natl Acad Sci U S A 119:e2204574119. https://doi.org/10.1073/pnas.2204574119
[12]
Gao H, Xie W, Yang C, Xu J, Li J, Wang H, Chen X, Huang CF (2018) NRAMP2, a trans-Golgi network-localized manganese transporter, is required for Arabidopsis root growth under manganese deficiency. New Phytol 217;179–193.
[13]
Guo J, Long L, Chen A, Dong X, Liu Z, Chen L, Wang J, Yuan L (2022) Tonoplast-localized transporter ZmNRAMP2 confers root-to-shoot translocation of manganese in maize. Plant Physiol 190:2601–2616. https://doi.org/10.1093/plphys/kiac434
[14]
Huai B, Yang Q, Qian Y, Qian W, Kang Z, Liu J (2019) ABA-induced sugar transporter TaSTP6 promotes wheat susceptibility to stripe rust. Plant Physiol 181:1328–1343. https://doi.org/10.1104/pp.19.00632
[15]
Huang C (2022) Ca2+ signaling in plant manganese uptake: CPK21/23 kinases phosphorylate and activate manganese transporter NRAMP1. Stress Biol 2:43. https://doi.org/10.1007/s44154-022-00067-w
[16]
JuC, ZhangZ, DengJ, MiaoC, WangZ, WallradL, JavedL, FuD, ZhangT, KudlaJ, et al.. Ca(2+)-dependent successive phosphorylation of vacuolar transporter MTP8 by CBL2/3-CIPK3/9/26 and CPK5 is critical for manganese homeostasis in Arabidopsis. Mol Plant, 2022, 15: 419-437
CrossRef Google scholar
[17]
KhanI, GratzR, DenezhkinP, Schott-VerdugoSN, AngrandK, GendersL, BasgaranRM, Fink-StraubeC, BrumbarovaT, GohlkeH, et al.. Calcium-promoted interaction between the C2-domain protein EHB1 and metal transporter IRT1 inhibits Arabidopsis iron acquisition. Plant Physiol, 2019, 180: 1564-1581
CrossRef Google scholar
[18]
LanquarV, LelièvreF, BolteS, HamèsC, AlconC, NeumannD, VansuytG, CurieC, SchröderA, KrämerU, et al.. Mobilization of vacuolar iron by AtNRAMP3 and AtNRAMP4 is essential for seed germination on low iron. EMBO J, 2005, 24: 4041-4051
CrossRef Google scholar
[19]
LanquarV, RamosMS, LelièvreF, Barbier-BrygooH, Krieger-LiszkayA, KrämerU, ThomineS. Export of vacuolar manganese by AtNRAMP3 and AtNRAMP4 is required for optimal photosynthesis and growth under manganese deficiency. Plant Physiol, 2010, 152: 1986-1999
CrossRef Google scholar
[20]
LeeS, LeeJ, RicachenevskyFK, PunshonT, TapperoR, SaltDE, GuerinotML. Redundant roles of four ZIP family members in zinc homeostasis and seed development in Arabidopsis thaliana. Plant J, 2021, 108: 1162-1173
CrossRef Google scholar
[21]
LiJ, JiaY, DongR, HuangR, LiuP, LiX, WangZ, LiuG, ChenZ. Advances in the mechanisms of plant tolerance to manganese toxicity. Int J Mol Sci, 2019, 20: 5096
CrossRef Google scholar
[22]
LiL, ZhuZ, LiaoY, YangC, FanN, ZhangJ, YamajiN, DirickL, MaJF, CurieC, et al.. NRAMP6 and NRAMP1 cooperatively regulate root growth and manganese translocation under manganese deficiency in Arabidopsis. Plant J, 2022, 110: 1564-1577
CrossRef Google scholar
[23]
Liu Y, Zhang Y, Wang Z, Guo S, Fang Y, Zhang Z, Gao H, Ren H, Wang C (2023) Plasma membrane-associated calcium signaling regulates arsenate tolerance in Arabidopsis. Plant Physiol 192:910-926. https://doi.org/10.1093/plphys/kiad171
[24]
Manishankar P, Wang N, Köster P, Alatar AA, Kudla J (2018) Calcium Signaling during Salt Stress and in the Regulation of Ion Homeostasis. J Exp Bot 69;4215–4226.
[25]
MilnerMJ, SeamonJ, CraftE, KochianLV. Transport properties of members of the ZIP family in plants and their role in Zn and Mn homeostasis. J Exp Bot, 2013, 64: 369-381
CrossRef Google scholar
[26]
PengF, WangC, ChengY, KangH, FanX, ShaL, ZhangH, ZengJ, ZhouY, WangY. Cloning and characterization of TpNRAMP3, a metal transporter from polish wheat (Triticum polonicum L.). Front Plant Sci, 2018, 9: 1354
CrossRef Google scholar
[27]
SasakiA, YamajiN, YokoshoK, MaJF. Nramp5 is a major transporter responsible for manganese and cadmium uptake in rice. Plant Cell, 2012, 24: 2155-2167
CrossRef Google scholar
[28]
SchmidtSB, HustedS. The biochemical properties of manganese in plants. Plants (basel, Switzerland), 2019, 8: 381
[29]
SchmidtSB, JensenPE, HustedS. Manganese deficiency in plants: the impact on photosystem II. Trends Plant Sci, 2016, 21: 622-632
CrossRef Google scholar
[30]
SochaAL, GuerinotML. Mn-euvering manganese: the role of transporter gene family members in manganese uptake and mobilization in plants. Front Plant Sci, 2014, 5: 106
CrossRef Google scholar
[31]
UenoD, SasakiA, YamajiN, MiyajiT, FujiiY, TakemotoY, MoriyamaS, CheJ, MoriyamaY, IwasakiK, et al.. A polarly localized transporter for efficient manganese uptake in rice. Nature Plants, 2015, 1: 15170
CrossRef Google scholar
[32]
WangN, TangC, FanX, HeM, GanP, ZhangS, HuZ, WangX, YanT, ShuW, et al.. Inactivation of a wheat protein kinase gene confers broad-spectrum resistance to rust fungi. Cell, 2022, 185: 2961-2974.e2919
CrossRef Google scholar
[33]
Wang Z, Zhang Y, Liu Y, Fu D, You Z, Huang P, Gao H, Zhang Z, Wang C (2023) Calcium-dependent protein kinases CPK21 and CPK23 phosphorylate and activate IRT1 to regulate iron deficiency in Arabidopsis. Sci China Life Sci. https://doi.org/10.1007/s11427-022-2330-4
[34]
Xie D, Ma X, Zhao Y, Li J, Fu D, Zhang Z, Ju C, Wang C (2023) Absorption, transport and regulation of manganese in plants. Sci China Vitae. https://doi.org/10.1360/SSV-2023-0027
[35]
YooSD, ChoYH, SheenJ. Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat Protoc, 2007, 2: 1565-1572
CrossRef Google scholar
[36]
ZhangB, ZhangC, LiuC, JingY, WangY, JinL, YangL, FuA, ShiJ, ZhaoF, et al.. Inner envelope CHLOROPLAST MANGANESE TRANSPORTER 1 supports manganese homeostasis and phototrophic growth in Arabidopsis. Mol Plant, 2018, 11: 943-954
CrossRef Google scholar
[37]
ZhangB, ZhangC, LiuC, FuA, LuanS. A Golgi-localized manganese transporter functions in pollen tube tip growth to control male fertility in Arabidopsis. Plant Commun, 2021, 2
CrossRef Google scholar
[38]
ZhangZ, FuD, SunZ, JuC, MiaoC, WangZ, XieD, MaL, GongZ, WangC. Tonoplast-associated calcium signaling regulates manganese homeostasis in Arabidopsis. Mol Plant, 2021, 14: 805-819
CrossRef Google scholar
[39]
ZhangY, WangZ, LiuY, ZhangT, LiuJ, YouZ, HuangP, ZhangZ, WangC. Plasma membrane-associated calcium signaling modulates cadmium transport. New Phytol, 2023, 238: 313-331
CrossRef Google scholar
[40]
ZhangZ, FuD, XieD, WangZ, ZhaoY, MaX, HuangP, JuC, WangC. CBL1/9-CIPK23-NRAMP1 axis regulates manganese toxicity. New Phytol, 2023, 239: 660-672
CrossRef Google scholar
Funding
National Natural Science Foundation of China(31900236)

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