Genetically modified trees with improved abiotic stress resistance - recent accomplishments. A review.

Anwar A., Kim J.-K., 2020. Transgenic breeding approaches for improving abiotic stress tolerance: recent progress and future perspectives. Int. J. Mol. Sci. 21(8), 2695. https://doi.org/10.3390/ijms21082695 DOI: https://doi.org/10.3390/ijms21082695

Bakhsh A., Hussain T., 2015. Engineering crop plants against abiotic stress: current achievements and prospects. Emir. J. Food Agric. 27(1), 24–39. https://doi.org/10.9755/ejfa.v27i1.17980 DOI: https://doi.org/10.9755/ejfa.v27i1.17980

Bian Z., Wang X., Lu J., Wang D., Zhou Y., Liu Y., Wang S., Yu Z., Xu D., Meng S., 2021. The yellowhorn AGL transcription factor gene XsAGL22 contributes to ABA biosynthesis and drought tolerance in poplar. Tree Physiol. 42(6), 1–14. https://doi.org/10.1093/treephys/tpab140 DOI: https://doi.org/10.1093/treephys/tpab140

Brodribb T.J., Powers J., Cochard H., Choat B., 2020. Hanging by a thread? Forests and drought. Science 368(6488), 261–266. https://doi.org/10.1126/science.aat7631 DOI: https://doi.org/10.1126/science.aat7631

Castro‐Rodríguez V., García‐Gutiérrez A., Canales J., Cañas R.A., Kirby E.G., Avila C., Cánovas F.M., 2016. Poplar trees for phytoremediation of high levels of nitrate and applications in bioenergy. Plant Biotechnol. J. 14(1), 299–312. https://doi.org/10.1111/pbi.12384 DOI: https://doi.org/10.1111/pbi.12384

Chang S., Mahon E.L., MacKay H.A., Rottmann W.H., Strauss S.H., Pijut P.M., Powell W.A., Coffey V., Lu H., Mansfield S.D., Jones T.J., 2018. Genetic engineering of trees: progress and new horizons. In Vitro Cell. Dev. Biol. Plant 54(4), 341–376. https://doi.org/10.1007/s11627-018-9914-1 DOI: https://doi.org/10.1007/s11627-018-9914-1

Cheng Z., Zhang X., Zhao K., Yao W., Li R., Zhou B., Jiang T., 2019. Over-expression of ERF38 gene enhances salt and osmotic tolerance in transgenic poplar. Front. Plant Sci. 10, 1375. https://doi.org/10.3389/fpls.2019.01375 DOI: https://doi.org/10.3389/fpls.2019.01375

Cortés A.J., Restrepo-Montoya M., Bedoya-Canas L.E., 2020. Modern strategies to assess and breed forest tree adaptation to changing climate. Front. Plant Sci. 11, 1606. https://doi.org/10.3389/fpls.2020.583323 DOI: https://doi.org/10.3389/fpls.2020.583323

DalCorso G., Martini F., Fasani E., Manara A., Visioli G., Furini A., 2021. Enhancement of Zn tolerance and accumulation in plants mediated by the expression of Saccharomyces cerevisiae vacuolar transporter ZRC1. Planta 253(6), 1–17. https://doi.org/10.1007/s00425-021-03634-z DOI: https://doi.org/10.1007/s00425-021-03634-z

dos Santos T.B., Ribas A.F., de Souza S.G.H., Budzinski I.G.F., Domingues D.S., 2022. Physiological responses to drought, salinity, and heat stress in plants: a review. Stresses 2(1), 113–135. https://doi.org/10.3390/stresses2010009 DOI: https://doi.org/10.3390/stresses2010009

Fillatti J.J., Sellmer J., McCown B., Haissig B., Comai L., 1987. Agrobacterium mediated transformation and regeneration of Populus. Mol. Gen. Genet. 206(2), 192–199. https://doi.org/10.1007/BF00333574 DOI: https://doi.org/10.1007/BF00333574

Geng X., Chen S., Yilan E., Zhang W., Mao H., Gigige A., Wang Y., Qi Z., Lin X., 2020. Overexpression of a tonoplast Na+/H+ antiporter from the halophytic shrub Nitraria sibirica improved salt tolerance and root development in transgenic poplar. Tree Genet. Genom. 16(6), 1–14. https://doi.org/10.1007/s11295-020-01475-7 DOI: https://doi.org/10.1007/s11295-020-01475-7

Guo Q., Jiang J., Yao W., Li L., Zhao K., Cheng Z., Han L., Wei R., Zhou B., Jiang T., 2021. Genome-wide analysis of poplar HD-Zip family and over-expression of PsnHDZ63 confers salt tolerance in transgenic Populus simonii × P. nigra. Plant Sci. 311, 111021. https://doi.org/10.1016/j.plantsci.2021.111021 DOI: https://doi.org/10.1016/j.plantsci.2021.111021

Häggman H., Sutela S., Fladung M., 2016. Genetic engineering contribution to forest tree breeding efforts. In: C. Vettori, F. Gallardo, H. Häggman, V. Kazana, F. Migliacci, G. Pilate, M. Fladung (eds.). Biosafety of forest transgenic trees. Springer, Dordrecht, 82, 11–29. https://doi.org/10.1007/978-94-017-7531-1_2 DOI: https://doi.org/10.1007/978-94-017-7531-1_2

He F., Li H. G., Wang J.J., Su Y., Wang H.L., Feng C.H., Yang Y., Niu M.-X., Liu C., Xia X., 2019. PeSTZ1, a C2H2‐type zinc finger transcription factor from Populus euphratica, enhances freezing tolerance through modulation of ROS scavenging by directly regulating PeAPX2. Plant Biotechnol. J. 17(11), 2169–2183. https://doi.org/10.1111/pbi.13130 DOI: https://doi.org/10.1111/pbi.13130

He F., Niu M.X., Feng C.H., Li H.G., Su Y., Su W.L., Pang H., Yang Y., Yu X., Wang H.-L., Wang J., Liu C., Yin W., Xia X., 2020. PeSTZ1 confers salt stress tolerance by scavenging the accumulation of ROS through regulating the expression of PeZAT12 and PeAPX2 in Populus. Tree Physiol. 40(9), 1292–1311. https://doi.org/10.1093/treephys/tpaa050 DOI: https://doi.org/10.1093/treephys/tpaa050

He F., Wang H.L., Li H.G., Su Y., Li S., Yang Y., Feng C.-H., Yin W., Xia X., 2018. Pe CHYR 1, a ubiquitin E3 ligase from Populus euphratica, enhances drought tolerance via ABA‐induced stomatal closure by ROS production in Populus. Plant Biotechnol. J. 16(8), 1514–1528. https://doi.org/10.1111/pbi.12893 DOI: https://doi.org/10.1111/pbi.12893

Huang S., Chen C., Xu M., Wang G., Xu L.A., Wu Y., 2021. Overexpression of Ginkgo BBX25 enhances salt tolerance in transgenic Populus. Plant Physiol. Biochem. 167, 946–954. https://doi.org/10.1016/j.plaphy.2021.09.021 DOI: https://doi.org/10.1016/j.plaphy.2021.09.021

Kim M.-H., Cho J.-S., Park E.-J., Lee H., Choi Y.-I., Bae E.-K., Han K.-H., Ko J.-H., 2020. Overexpression of a poplar Ring-H2 zinc finger, Ptxerico, confers enhanced drought tolerance via

reduced water loss and ion leakage in Populus. Int. J. Mol. Sci. 21(24), 9454. https://doi.org/10.3390/ijms21249454 DOI: https://doi.org/10.3390/ijms21249454

Lebedev V.G., Popova A.A., Shestibratov K.A., 2021. Genetic engineering and genome editing for improving nitrogen use efficiency in plants. Cells 10(12), 3303. https://doi.org/10.3390/cells10123303 DOI: https://doi.org/10.3390/cells10123303

Li D., Yang J., Pak S., Zeng M., Sun J., Yu S., He Y., Li C., 2022. PuC3H35 confers drought tolerance by enhancing lignin and proanthocyanidin biosynthesis in the roots of Populus ussuriensis. New Phytol. 233(1), 390–408. https://doi.org/10.1111/nph.17799 DOI: https://doi.org/10.1111/nph.17799

Llanes A., Palchetti M.V., Vilo C., Ibañez C., 2021. Molecular control to salt tolerance mechanisms of woody plants: recent achievements and perspectives. Ann. For. Sci. 78(4), 1–19. https://doi.org/10.1007/s13595-021-01107-7 DOI: https://doi.org/10.1007/s13595-021-01107-7

Meng S., Cao Y., Li H., Bian Z., Wang D., Lian C., Yin W., Xia X., 2019. PeSHN1 regulates water-use efficiency and drought tolerance by modulating wax biosynthesis in poplar. Tree Physiol. 39(8), 1371–1386. https://doi.org/10.1093/treephys/tpz033 DOI: https://doi.org/10.1093/treephys/tpz033

Moran E., Lauder J., Musser C., Stathos A., Shu M., 2017. The genetics of drought tolerance in conifers. New Phytol. 216(4), 1034–1048. https://doi.org/10.1111/nph.14774 DOI: https://doi.org/10.1111/nph.14774

Nagle M., Déjardin A., Pilate G., Strauss S.H., 2018. Opportunities for innovation in genetic transformation of forest trees. Front. Plant Sci. 9, 1443. https://doi.org/10.3389/fpls.2018.01443 DOI: https://doi.org/10.3389/fpls.2018.01443

Neri A., Traversari S., Andreucci A., Francini A., Sebastiani L., 2020. The role of aquaporin overexpression in the modulation of transcription of heavy metal transporters under cadmium treatment in poplar. Plants 10(1), 54. https://doi.org/10.3390/plants10010054 DOI: https://doi.org/10.3390/plants10010054

Nguyen H.C., Lin K.H., Ho S.L., Chiang C.M., Yang C.M., 2018. Enhancing the abiotic stress tolerance of plants: from chemical treatment to biotechnological approaches. Physiol. Plant. 164(4), 452–466. https://doi.org/10.1111/ppl.12812 DOI: https://doi.org/10.1111/ppl.12812

Nowicka B., Ciura J., Szymańska R., Kruk J., 2018. Improving photosynthesis, plant productivity and abiotic stress tolerance – current trends and future perspectives. J. Plant Physiol. 231, 415–433. https://doi.org/10.1016/j.jplph.2018.10.022 DOI: https://doi.org/10.1016/j.jplph.2018.10.022

Ozyigit I.I., Can H., Dogan I., 2021. Phytoremediation using genetically engineered plants to remove metals: a review. Environ. Chem. Lett. 19(1), 669–698. https://doi.org/10.1007/s10311-020-01095-6 DOI: https://doi.org/10.1007/s10311-020-01095-6

Polle A., Chen S.L., Eckert C., Harfouche A., 2019. Engineering drought resistance in forest trees. Front. Plant Sci. 9, 1875. https://doi.org/10.3389/fpls.2018.01875 DOI: https://doi.org/10.3389/fpls.2018.01875

Rai P.K., Kim K.H., Lee S.S., Lee J.H., 2020. Molecular mechanisms in phytoremediation of environmental contaminants and prospects of engineered transgenic plants/microbes. Sci. Total Environ. 705, 135858. https://doi.org/10.1016/j.scitotenv.2019.135858 DOI: https://doi.org/10.1016/j.scitotenv.2019.135858

Rajput V.D., Singh R.K., Verma K.K., Sharma L., Quiroz-Figueroa F.R., Meena M., Gour V.S., Minkina T., Sushkova S., Mandzhieva S., 2021. Recent developments in enzymatic antioxidant defence mechanism in plants with special reference to abiotic stress. Biology 10(4), 267. https://doi.org/10.3390/biology10040267 DOI: https://doi.org/10.3390/biology10040267

Sharma P., Sharma M.M.M., Patra A., Vashisth M., Mehta S., Singh B., Tiwari M., Pandey V., 2020. The role of key transcription factors for cold tolerance in plants. In: S.H. Wani (ed.). Transcription factors for abiotic stress tolerance in plants. Academic Press. 123–152. https://doi.org/10.1016/B978-0-12-819334-1.00009-5 DOI: https://doi.org/10.1016/B978-0-12-819334-1.00009-5

Shen C., Zhang Y., Li Q., Liu S., He F., An Y., Zhou Y., Liu C., Tin W., Xia X., 2021. PdGNC confers drought tolerance by mediating stomatal closure resulting from NO and H2O2 production via the direct regulation of PdHXK1 expression in Populus. New Phytol. 230(5), 1868–1882. https://doi.org/10.1111/nph.17301 DOI: https://doi.org/10.1111/nph.17301

Sun L., Ma Y., Wang H., Huang W., Wang X., Han L., Sun W., Han E., Wang B., 2018. Overexpression of PtABCC1 contributes to mercury tolerance and accumulation in Arabidopsis and poplar. Biochem. Biophys. Res. Commun. 497(4), 997–1002. https://doi.org/10.1016/j.bbrc.2018.02.133 DOI: https://doi.org/10.1016/j.bbrc.2018.02.133

Thakur A.K., Kumar P., Parmar N., Shandil R.K., Aggarwal G., Gaur A., Srivastava D.K., 2021. Achievements and prospects of genetic engineering in poplar: a review. New For. 52(6), 889–920. https://doi.org/10.1007/s11056-021-09836-3 DOI: https://doi.org/10.1007/s11056-021-09836-3

Wang S., Fan Y., Du S., Zhao K., Liu Q., Yao W., Zheg T., Han Y., 2022. PtaERF194 inhibits plant growth and enhances drought tolerance in poplar. Tree Physiol. 42(8), 1678–1692. https://doi.org/10.1093/treephys/tpac026 DOI: https://doi.org/10.1093/treephys/tpac026

Wang X., Movahedi A., Wei H., Wu X., Zhang J., Sun W., Li D., Zhuge Q., 2020. Overexpression of PtAnnexin1 from Populus trichocarpa enhances salt and drought tolerance in transgenic poplars. Tree Genet. Genomes, 16(1), 1–13. https://doi.org/10.1007/s11295-020-1412-z DOI: https://doi.org/10.1007/s11295-020-1412-z

Wang Y.-M., Zhang Y.-M., Zhang X., Zhao X., Zhang Y., Wang C., Wang Y.-C., Wang L.-Q., 2021. Poplar PsnICE1 enhances cold tolerance by binding to different cis-acting elements to improve reactive oxygen species-scavenging capability. Tree Physiol. 41(12), 2424–2437. https://doi.org/10.1093/treephys/tpab084 DOI: https://doi.org/10.1093/treephys/tpab084

Wei H., Movahedi A., Xu C., Wang P., Sun W., Yin T., Zhuge Q., 2019. Heterologous overexpression of the Arabidopsis SnRK2. 8 gene enhances drought and salt tolerance in Populus × euramericana cv ‘Nanlin895’. Plant Biotechnol. Rep. 13(3), 245–261. https://doi.org/10.1007/s11816-019-00531-6 DOI: https://doi.org/10.1007/s11816-019-00531-6

Wu X., Chen Q., Chen L., Tian F., Chen X., Han C., Mi J., Lin X., Wan X., Jiang B., Liu Q., Chen L., Zhang F., 2022. A WRKY transcription factor, PyWRKY75, enhanced cadmium accumulationand tolerance in poplar. Ecotoxicol. Environ. Saf., 239, 113630. https://doi.org/10.1016/j.ecoenv.2022.113630 DOI: https://doi.org/10.1016/j.ecoenv.2022.113630

Xin Y., Wu Y., Han X., Xu L.A., 2021. Overexpression of the Ginkgo biloba WD40 gene GbLWD1-like improves salt tolerance in transgenic Populus. Plant Sci. 313, 111092. https://doi.org/10.1016/j.plantsci.2021.111092 DOI: https://doi.org/10.1016/j.plantsci.2021.111092

Xu M., Chen C., Cai H., Wu L., 2018. Overexpression of PeHKT1; 1 improves salt tolerance in Populus. Genes 9(10), 475. https://doi.org/10.3390/genes9100475 DOI: https://doi.org/10.3390/genes9100475

Yadav R., Yadav N., Goutam U., Kumar S., Chaudhury A., 2017. Genetic engineering of poplar: current achievements and future goals. In: S. Gahlawat, R. Salar, P. Siwach, J. Duhan, S. Kumar, P. Kaur (eds.). Plant biotechnology: recent advancements and developments. Springer, Singapore, 361–390. https://doi.org/10.1007/978-981-10-4732-9_17 DOI: https://doi.org/10.1007/978-981-10-4732-9_17

Yang Y., Li H.-G., Wang J., Wang H.-L., He F., Su Y., Zhang Y., Feng C.-H., Niu M., Li Z., Yin W., Xia X., 2020. ABF3 enhances drought tolerance via promoting ABA-induced stomatal closure by directly regulating ADF5 in Populus euphratica. J. Exp. Bot. 71(22), 7270–7285. https://doi.org/10.1093/jxb/eraa383 DOI: https://doi.org/10.1093/jxb/eraa383

Zhang H., Yang J., Li W., Chen Y., Lu H., Zhao S., Li D., Wei M., Li C., 2019. PuHSFA4a enhances tolerance to excess zinc by regulating reactive oxygen species production and root development in Populus. Plant Physiol. 180(4), 2254–2271. https://doi.org/10.1104/pp.18.01495 DOI: https://doi.org/10.1104/pp.18.01495

Zhang M., Liu Y., Han G., Zhang Y., Wang B., Chen M., 2021. Salt tolerance mechanisms in trees: research progress. Trees 35(3), 717–730. https://doi.org/10.1007/s00468-020-02060-0 DOI: https://doi.org/10.1007/s00468-020-02060-0

Zhao H., Zhao X., Li M., Jiang Y., Xu J., Jin J., Li K., 2018. Ectopic expression of Limonium bicolor (Bag.) Kuntze DREB (LbDREB) results in enhanced salt stress tolerance of transgenic Populus ussuriensis Kom. Plant Cell Tissue Organ Cult., 132(1), 123–136. https://doi.org/10.1007/s11240-017-1317-1 DOI: https://doi.org/10.1007/s11240-017-1317-1