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Overexpression of TaLAX3-1B alters the stomatal aperture and improves the salt stress resistance of tobacco

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Abstract

Background

Stomata, which play important roles in both optimizing photosynthesis efficiency and adapting to stress, are closely related to IAA and ABA. In plants, the auxin influx carrier LAX3 has been found to play roles in development and stress tolerance. However, the function of LAX3 in stomata and in response to salt stress remains largely unknown.

Methods and results

Here, we show that overexpression of wheat TaLAX3-1B in tobacco results in a decrease in stomatal aperture and a relatively closed state of the stomata. In addition, the stomatal movement of the OxTaLAX3-1B lines was less sensitive to ABA than that of the WT. Consistently, compared with the WT, the OxTaLAX3-1B lines showed significantly higher expression of stomate-, IAA- and ABA-related genes and endogenous IAA and ABA contents. Furthermore, compared with the WT, the OxTaLAX3-1B lines exhibited higher proline content, salt stress-related gene expression and ROS antioxidant enzyme activity but lower MDA content and ROS accumulation after salt treatment.

Conclusions

The present results suggest that TaLAX3-1B plays a positive role in regulating stomatal closure and enhancing salt stress tolerance.

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References

  1. Zhang JY, He SB, Li L, Yang HQ (2014) Auxin inhibits stomatal development through MONOPTEROS repression of a mobile peptide gene STOMAGEN in mesophyll. PNAS 111(29):E3015-3023. https://doi.org/10.1073/pnas.1400542111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Hosotani S, Yamauchi S, Kobayashi H, Fuji S, Koya S, Shimazaki KI, Takemiya A (2021) A BLUS1 kinase signal and a decrease in intercellular CO2 concentration are necessary for stomatal opening in response to blue light. Plant Cell 33(5):1813–1827. https://doi.org/10.1093/plcell/koab067

    Article  PubMed  PubMed Central  Google Scholar 

  3. Qi J, Song CP, Wang B, Zhou J, Kangasjärvi J, Zhu JK, Gong Z (2018) Reactive oxygen species signaling and stomatal movement in plant responses to drought stress and pathogen attack. J Integr Plant Biol 60(9):805–826. https://doi.org/10.1111/jipb.12654

    Article  CAS  PubMed  Google Scholar 

  4. Ma S, Zhou X, Jahan MS, Guo S, Tian M, Zhou R, Liu H, Feng B, Shu S (2022) Putrescine regulates stomatal opening of cucumber leaves under salt stress via the H2O2-mediated signaling pathway. Plant Physiol Biochem 170:87–97. https://doi.org/10.1016/j.plaphy.2021.11.028

    Article  CAS  PubMed  Google Scholar 

  5. Jalakas P, Merilo E, Kollist H, Brosché M (2018) ABA-mediated regulation of stomatal density is OST1-independent. Plant Direct 2(9):e00082. https://doi.org/10.1002/pld3.82

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Wei H, Jing Y, Zhang L, Kong D (2021) Phytohormones and their crosstalk in regulating stomatal development and patterning. J Exp Bot 72(7):2356–2370. https://doi.org/10.1093/jxb/erab034

    Article  CAS  PubMed  Google Scholar 

  7. Lohse G, Hedrich R (1992) Characterization of the plasma-membrane H+-ATPase from Vicia faba guard cells. Planta 188:206–214. https://doi.org/10.1007/BF00216815

    Article  CAS  PubMed  Google Scholar 

  8. Balcerowicz M, Ranjan A, Rupprecht L, Fiene G, Hoecker U (2014) Auxin represses stomatal development in dark-grown seedlings via Aux/IAA proteins. Development 141(16):3165–3176. https://doi.org/10.1242/dev.109181

    Article  CAS  PubMed  Google Scholar 

  9. Batista-Silva W, Medeiros DB, Rodrigues-Salvador A, Daloso DM, Omena-Garcia RP, Oliveira FS, Pino LE, Peres LEP, Nunes-Nesi A, Fernie AR, Zsögön A, Araújo WL (2018) Modulation of auxin signalling through DIAGETROPICA and ENTIRE differentially affects tomato plant growth via changes in photosynthetic and mitochondrial metabolism. Plant Cell Environ 42(2):448–465. https://doi.org/10.1111/pce.13413

    Article  CAS  PubMed  Google Scholar 

  10. Salehin M, Li B, Tang M, Katz E, Song L, Ecker JR, Kliebenstein DJ, Estelle M (2019) Auxin-sensitive Aux/IAA proteins mediate drought tolerance in Arabidopsis by regulating glucosinolate levels. Nat Commun 10(1):4021. https://doi.org/10.1038/s41467-019-12002-1

    Article  PubMed  PubMed Central  Google Scholar 

  11. Acharya BR, Assmann SM (2009) Hormone interactions in stomatal function. Plant Mol Biol 69(4):451–462. https://doi.org/10.1007/s11103-008-9427-0

    Article  CAS  PubMed  Google Scholar 

  12. Bouzroud S, Gasparini K, Hu G, Barbosa MAM, Rosa BL, Fahr M, Bendaou N, Bouzayen M, Zsögön A, Smouni A, Zouine M (2020) Down regulation and loss of auxin response factor 4 function using CRISPR/Cas9 alters plant growth, stomatal function and improves tomato tolerance to salinity and osmotic stress. Genes (Basel) 11(3):272. https://doi.org/10.3390/genes11030272

    Article  CAS  Google Scholar 

  13. He Y, Liu Y, Li M, Lamin-Samu AT, Yang D, Yu X, Izhar M, Jan I, Ali M, Lu G (2021) The Arabidopsis SMALL AUXIN UP RNA32 protein regulates ABA-mediated responses to drought stress. Front Plant Sci 12:625493. https://doi.org/10.3389/fpls.2021.625493

    Article  PubMed  PubMed Central  Google Scholar 

  14. Porco S, Larrieu A, Du Y, Gaudinier A, Goh T, Swarup K, Swarup R, Kuempers B, Bishopp A, Lavenus J, Casimiro I, Hill K, Benkova E, Fukaki H, Brady SM, Scheres B, Péret B, Bennett MJ (2016) Lateral root emergence in Arabidopsis is dependent on transcription factor LBD29 regulation of auxin influx carrier LAX3. Development 143(18):3340–3349. https://doi.org/10.1242/dev.136283

    Article  CAS  PubMed  Google Scholar 

  15. Vandenbussche F, Petrásek J, Zádníková P, Hoyerová K, Pesek B, Raz V, Swarup R, Bennett M, Zazímalová E, Benková E, Van Der Straeten D (2010) The auxin influx carriers AUX1 and LAX3 are involved in auxin-ethylene interactions during apical hook development in Arabidopsis thaliana seedlings. Development 137(4):597–606. https://doi.org/10.1242/dev.040790

    Article  CAS  PubMed  Google Scholar 

  16. Basu MM, González-Carranza ZH, Azam-Ali S, Tang S, Shahid AA, Roberts JA (2013) The manipulation of auxin in the abscission zone cells of Arabidopsis flowers reveals that indoleacetic acid signaling is a prerequisite for organ shedding. Plant Physiol 162(1):96–106. https://doi.org/10.1104/pp.113.216234

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Yu Q, Zhang Y, Wang J, Yan X, Wang C, Xu J, Pan J (2016) Clathrin-mediated auxin efflux and maxima regulate hypocotyl hook formation and light-stimulated hook opening in Arabidopsis. Mol Plant 9(1):101–112. https://doi.org/10.1016/j.molp.2015.09.018

    Article  CAS  PubMed  Google Scholar 

  18. An H, Zhang J, Xu F, Jiang S, Zhang X (2020) Transcriptomic profiling and discovery of key genes involved in adventitious root formation from green cuttings of highbush blueberry (Vaccinium corymbosum L.). BMC Plant Biol 20(1):182. https://doi.org/10.1186/s12870-020-02398-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Yan F, Gong Z, Hu G, Ma X, Bai R, Yu R, Zhang Q, Deng W, Li Z, Wuriyanghan H (2021) Tomato SlBL4 plays an important role in fruit pedicel organogenesis and abscission. Hortic Res 8(1):78. https://doi.org/10.1038/s41438-021-00515-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Wu B, Li N, Deng Z, Luo F, Duan Y (2021) Selection and evaluation of a thornless and HLB-tolerant bud-sport of pummelo citrus with an emphasis on molecular mechanisms. Front Plant Sci 12:739108. https://doi.org/10.3389/fpls.2021.739108

    Article  PubMed  PubMed Central  Google Scholar 

  21. Bahieldin A, Atef A, Edris S, Gadalla NO, Ramadan AM, Hassan SM, Al Attas SG, Al-Kordy MA, Al-Hajar ASM, Sabir JSM, Nasr ME, Osman GH, El-Domyati FM (2018) Multifunctional activities of ERF109 as affected by salt stress in Arabidopsis. Sci Rep 8(1):6403. https://doi.org/10.1038/s41598-018-24452-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Li F, Sun C, Li X, Yu X, Luo C, Shen Y, Qu S (2018) The effect of graphene oxide on adventitious root formation and growth in apple. Plant Physiol Biochem 129:122–129. https://doi.org/10.1016/j.plaphy.2018.05.029

    Article  CAS  PubMed  Google Scholar 

  23. Gao Y, Cui Y, Zhao R, Chen X, Zhang J, Zhao J, Kong L (2022) Cryo-treatment enhances the embryogenicity of aature somatic embryos via the lncRNA-miRNA-mRNA network in white spruce. Int J Mol Sci 23(3):1111. https://doi.org/10.3390/ijms23031111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Zhang K, Xia X, Zhang Y, Gan SS (2012) An ABA-regulated and Golgi-localized protein phosphatase controls water loss during leaf senescence in Arabidopsis. Plant J 69(4):667–678. https://doi.org/10.1111/j.1365-313X.2011.04821.x

    Article  CAS  PubMed  Google Scholar 

  25. Li CL, Wang M, Ma XY, Zhang W (2014) NRGA1, a putative mitochondrial pyruvate carrier, mediates ABA regulation of guard cell ion channels and drought stress responses in Arabidopsis. Mol Plant 7(10):1508–1521. https://doi.org/10.1093/mp/ssu061

    Article  CAS  PubMed  Google Scholar 

  26. Li LH, Yang GP, Ren MJ, Wang ZN, Peng YS, Xu RH (2021) Co-regulation of auxin and cytokinin in anthocyanin accumulation during natural development of purple wheat grains. J Plant Growth Regul 40(2021):1881–1893. https://doi.org/10.1007/s00344-020-10237-7

    Article  CAS  Google Scholar 

  27. Shahinnia F, Roy JL, Laborde B, Sznajder B, Kalambettu P, Mahjourimajd S, Tilbrook J, Fleury D (2016) Genetic association of stomatal traits and yield in wheat grown in low rainfall environments. BMC Plant Biol 16(1):150. https://doi.org/10.1186/s12870-016-0838-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Hedrich R, Geiger D (2017) Biology of SLAC1-type anion channels-from nutrient uptake to stomatal closure. New Phytol 216(1):46–61. https://doi.org/10.1111/nph.14685

    Article  CAS  PubMed  Google Scholar 

  29. Dittrich M, Mueller HM, Bauer H, Peirats-Llobet M, Rodriguez PL, Geilfus CM, Carpentier SC, Rasheid KASA, Kollist H, Merilo E, Herrmann J, Müller T, Ache P, Hetherington AM, Hedrich R (2019) The role of Arabidopsis ABA receptors from the PYR/PYL/RCAR family in stomatal acclimation and closure signal integration. Nat Plants 5(9):1002–1011. https://doi.org/10.1038/s41477-019-0490-0

    Article  CAS  PubMed  Google Scholar 

  30. Nurbekova Z, Srivastava S, Standing D, Kurmanbayeva A, Bekturova A, Soltabayeva A, Oshanova D, Turečková V, Strand M, Biswas MS, Mano J, Sagi M (2021) Arabidopsis aldehyde oxidase 3, known to oxidize abscisic aldehyde to abscisic acid, protects leaves from aldehyde toxicity. Plant J 108(5):1439–1455. https://doi.org/10.1111/tpj.15521

    Article  CAS  PubMed  Google Scholar 

  31. Zelm EV, Zhang Y, Testerink C (2020) Salt tolerance mechanisms of plants. Annu Re Plant Biol 71:403–433. https://doi.org/10.1146/annurev-arplant-050718-100005

    Article  CAS  Google Scholar 

  32. Yang Y, Guo Y (2018) Unraveling salt stress signaling in plants. J Integr Plant Biol 60(9):796–804. https://doi.org/10.1111/jipb.12689

    Article  CAS  PubMed  Google Scholar 

  33. Kale L, Nakurte I, Jalakas P, Kunga-Jegere L, Brosché M, Rostoks N (2019) Arabidopsis mutant dnd2 exhibits increased auxin and abscisic acid content and reduced stomatal conductance. Plant Physiol Biochem 140:18–26. https://doi.org/10.1016/j.plaphy.2019.05.004

    Article  CAS  PubMed  Google Scholar 

  34. Zhu Z, Sun B, Xu X, Chen H, Zou L, Chen G, Cao B, Chen C, Lei J (2016) Overexpression of AtEDT1/HDG11 in Chinese kale (Brassica oleracea var. alboglabra) enhances drought and osmotic stress tolerance. Front Plant Sci 7:1285. https://doi.org/10.3389/fpls.2016.01285

    Article  PubMed  PubMed Central  Google Scholar 

  35. Jiao Q, Chen T, Niu G, Zhang H, Zhou C, Hong Z (2020) N-glycosylation is involved in stomatal development by modulating the release of active abscisic acid and auxin in Arabidopsis. J Exp Bot 71(19):5865–5879. https://doi.org/10.1093/jxb/eraa321

    Article  CAS  PubMed  Google Scholar 

  36. Fatma M, Iqbal N, Gautam H, Sehar Z, Sofo A, D’Ippolito I, Khan NA (2021) Ethylene and sulfur coordinately modulate the antioxidant system and ABA accumulation in mustard plants under salt stress. Plants (Basel) 10(1):180. https://doi.org/10.3390/plants10010180

    Article  CAS  Google Scholar 

  37. Hichri I, Muhovski Y, Žižková E, Dobrev PI, Gharbi E, Franco-Zorrilla JM, Lopez-Vidriero I, Solano R, Clippe A, Errachid A, Motyka V, Lutts S (2017) The Solanum lycopersicum WRKY3 transcription factor SlWRKY3 is involved in salt stress tolerance in tomato. Front Plant Sci 8:1343. https://doi.org/10.3389/fpls.2017.01343

    Article  PubMed  PubMed Central  Google Scholar 

  38. Kishor PBK, Sreenivasulu N (2014) Is proline accumulation per se correlated with stress tolerance or is proline homeostasis a more critical issue? Plant Cell Environ 37:300–311. https://doi.org/10.1111/pce.12157

    Article  CAS  Google Scholar 

  39. Gao YF, Liu JK, Yang FM, Zhang GY, Wang D, Zhang L, Ou YB, Yao YA (2020) The WRKY transcription factor WRKY8 promotes resistance to pathogen infection and mediates drought and salt stress tolerance in Solanum lycopersicum. Physiol Plant 168(1):98–117. https://doi.org/10.1111/ppl.12978

    Article  CAS  PubMed  Google Scholar 

  40. Zhang H, Zhai J, Mo J, Li D, Song F (2012) Overexpression of rice sphingosine-1-phoshpate lyase gene OsSPL1 in transgenic tobacco reduces salt and oxidative stress tolerance. J Integr Plant Biol 54(9):652–662. https://doi.org/10.1111/j.1744-7909.2012.01150.x

    Article  CAS  PubMed  Google Scholar 

  41. Li JB, Luan YS, Liu Z (2015) Overexpression of SpWRKY1 promotes resistance to Phytophthora nicotianae and tolerance to salt and drought stress in transgenic tobacco. Physiol Plant 155(3):248–266. https://doi.org/10.1111/ppl.12315

    Article  CAS  PubMed  Google Scholar 

  42. van Zelm E, Zhang Y, Testerink C (2020) Salt tolerance mechanisms of plants. Annu Rev Plant Biol 71:403–433. https://doi.org/10.1146/annurev-arplant-050718-100005

    Article  CAS  PubMed  Google Scholar 

  43. Nakabayashi R, Yonekura-Sakakibara K, Urano K, Suzuki M, Yamada Y, Nishizawa T (2014) Enhancement of oxidative and drought tolerance in Arabidopsis by overaccumulation of antioxidant flavonoids. Plant J 77:367–379. https://doi.org/10.1111/tpj.12388

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We thank Springer (https://secure.authorservices.springernature.com/en/default/submit/select) for editing this manuscript.

Funding

This project was supported by grants from the Guizhou Science and Technology Plan Project ([2020] 1Z018), Guizhou Science and Technology Support Project ([2021] YiBan272), National Natural Science Foundation of China (32160456), and Guizhou Science and Technology Plan Project ([2019] 1073).

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Authors and Affiliations

  1. College of Agriculture, Guizhou University, Guiyang, 550025, China

    Luhua Li, Dingli Hong, Chang An, Yuxuan Chen, Pengpeng Zhao, Xin Li, Fumin Xiong, Mingjian Ren & Ruhong Xu

  2. Guizhou Sub-Center of National Wheat Improvement Center, Guiyang, 550025, China

    Luhua Li, Dingli Hong, Chang An, Yuxuan Chen, Pengpeng Zhao, Xin Li, Fumin Xiong, Mingjian Ren & Ruhong Xu

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  1. Luhua Li
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Contributions

CA performed the experiments; DH, YC and PZ participated in qRT-PCR data analysis; XL, FX and MR collected the data; RX and LL designed the study; and LL and RX wrote the manuscript.

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Correspondence to Ruhong Xu.

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Li, L., Hong, D., An, C. et al. Overexpression of TaLAX3-1B alters the stomatal aperture and improves the salt stress resistance of tobacco. Mol Biol Rep 49, 7455–7464 (2022). https://doi.org/10.1007/s11033-022-07548-1

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