Glucose Uptake from the Rhizosphere Mediated by MdDOF3-MdHT1.2 Regulates Drought Resistance in Apple

Overview

Journal Plant Biotechnol J

Specialties Biology
Biotechnology

Date 2024 Jan 11

PMID 38205680

Authors

Xiaocheng Tian

Yuxing Li

Shaoteng Wang

Hui Zou

Qian Xiao

Baiquan Ma

Fengwang Ma

Mingjun Li

Affiliations

Soon will be listed here.

Abstract

In plants under drought stress, sugar content in roots increases, which is important for drought resistance. However, the molecular mechanisms for controlling the sugar content in roots during response to drought remain elusive. Here, we found that the MdDOF3-MdHT1.2 module-mediated glucose influx into the root is essential for drought resistance in apple (Malus × domestica). Drought induced glucose uptake from the rhizosphere and up-regulated the transcription of hexose transporter MdHT1.2. Compared with the wild-type plants, overexpression of MdHT1.2 promoted glucose uptake from the rhizosphere, thereby facilitating sugar accumulation in root and enhancing drought resistance, whereas silenced plants showed the opposite phenotype. Furthermore, ATAC-seq, RNA-seq and biochemical analysis demonstrated that MdDOF3 directly bound to the promoter of MdHT1.2 and was strongly up-regulated under drought. Overexpression of MdDOF3 in roots improved MdHT1.2-mediated glucose transport capacity and enhanced plant resistance to drought, but MdDOF3-RNAihr apple plants showed the opposite phenotype. Moreover, overexpression of MdDOF3 in roots did not attenuate drought sensitivity in MdHT1.2-RNAi plants, which was correlated with a lower glucose uptake capacity and glucose content in root. Collectively, our findings deciphered the molecular mechanism through which glucose uptake from the rhizosphere is mediated by MdDOF3-MdHT1.2, which acts to modulate sugar content in root and promote drought resistance.

References

Li Y, Li Y, Cui Y, Xie Y, Shi Y, Shang Y . GABA-mediated inhibition of cadmium uptake and accumulation in apples. Environ Pollut. 2022; 300:118867. DOI: 10.1016/j.envpol.2022.118867. View

Reinders A, Sivitz A, Hsi A, Grof C, Perroux J, Ward J . Sugarcane ShSUT1: analysis of sucrose transport activity and inhibition by sucralose. Plant Cell Environ. 2006; 29(10):1871-80. DOI: 10.1111/j.1365-3040.2006.01563.x. View

Nishizawa A, Yabuta Y, Shigeoka S . Galactinol and raffinose constitute a novel function to protect plants from oxidative damage. Plant Physiol. 2008; 147(3):1251-63. PMC: 2442551. DOI: 10.1104/pp.108.122465. View

Yamada K, Kanai M, Osakabe Y, Ohiraki H, Shinozaki K, Yamaguchi-Shinozaki K . Monosaccharide absorption activity of Arabidopsis roots depends on expression profiles of transporter genes under high salinity conditions. J Biol Chem. 2011; 286(50):43577-86. PMC: 3234862. DOI: 10.1074/jbc.M111.269712. View

Thalmann M, Pazmino D, Seung D, Horrer D, Nigro A, Meier T . Regulation of Leaf Starch Degradation by Abscisic Acid Is Important for Osmotic Stress Tolerance in Plants. Plant Cell. 2016; 28(8):1860-78. PMC: 5006701. DOI: 10.1105/tpc.16.00143. View

Truernit E, Stadler R, Baier K, Sauer N . A male gametophyte-specific monosaccharide transporter in Arabidopsis. Plant J. 1999; 17(2):191-201. DOI: 10.1046/j.1365-313x.1999.00372.x. View

Li M, Li P, Ma F, Dandekar A, Cheng L . Sugar metabolism and accumulation in the fruit of transgenic apple trees with decreased sorbitol synthesis. Hortic Res. 2018; 5:60. PMC: 6269491. DOI: 10.1038/s41438-018-0064-8. View

Huai B, Yuan P, Ma X, Zhang X, Jiang L, Zheng P . Sugar transporter TaSTP3 activation by TaWRKY19/61/82 enhances stripe rust susceptibility in wheat. New Phytol. 2022; 236(1):266-282. DOI: 10.1111/nph.18331. View

Durand M, Porcheron B, Hennion N, Maurousset L, Lemoine R, Pourtau N . Water Deficit Enhances C Export to the Roots in Arabidopsis thaliana Plants with Contribution of Sucrose Transporters in Both Shoot and Roots. Plant Physiol. 2016; 170(3):1460-79. PMC: 4775148. DOI: 10.1104/pp.15.01926. View

10.

Taji T, Ohsumi C, Iuchi S, Seki M, Kasuga M, Kobayashi M . Important roles of drought- and cold-inducible genes for galactinol synthase in stress tolerance in Arabidopsis thaliana. Plant J. 2002; 29(4):417-26. DOI: 10.1046/j.0960-7412.2001.01227.x. View

11.

Zhu L, Li Y, Wang C, Wang Z, Cao W, Su J . The SnRK2.3-AREB1-TST1/2 cascade activated by cytosolic glucose regulates sugar accumulation across tonoplasts in apple and tomato. Nat Plants. 2023; 9(6):951-964. DOI: 10.1038/s41477-023-01443-8. View

12.

Wang H, Zhang B, Hao Y, Huang J, Tian A, Liao Y . The soybean Dof-type transcription factor genes, GmDof4 and GmDof11, enhance lipid content in the seeds of transgenic Arabidopsis plants. Plant J. 2007; 52(4):716-29. DOI: 10.1111/j.1365-313X.2007.03268.x. View

13.

Gifford R, Thorne J, Hitz W, Giaquinta R . Crop productivity and photoassimilate partitioning. Science. 1984; 225(4664):801-8. DOI: 10.1126/science.225.4664.801. View

14.

Tian X, Zou H, Xiao Q, Xin H, Zhu L, Li Y . Uptake of glucose from the rhizosphere, mediated by apple MdHT1.2, regulates carbohydrate allocation. Plant Physiol. 2023; 193(1):410-425. DOI: 10.1093/plphys/kiad221. View

15.

Kang H, Foley R, Onate-Sanchez L, Lin C, Singh K . Target genes for OBP3, a Dof transcription factor, include novel basic helix-loop-helix domain proteins inducible by salicylic acid. Plant J. 2003; 35(3):362-72. DOI: 10.1046/j.1365-313x.2003.01812.x. View

16.

An J, Li R, Qu F, You C, Wang X, Hao Y . R2R3-MYB transcription factor MdMYB23 is involved in the cold tolerance and proanthocyanidin accumulation in apple. Plant J. 2018; 96(3):562-577. DOI: 10.1111/tpj.14050. View

17.

Zou H, Zhang Y, Wei W, Chen H, Song Q, Liu Y . The transcription factor AtDOF4.2 regulates shoot branching and seed coat formation in Arabidopsis. Biochem J. 2012; 449(2):373-88. DOI: 10.1042/BJ20110060. View

18.

Chen H, Huh J, Yu Y, Ho L, Chen L, Tholl D . The Arabidopsis vacuolar sugar transporter SWEET2 limits carbon sequestration from roots and restricts Pythium infection. Plant J. 2015; 83(6):1046-58. DOI: 10.1111/tpj.12948. View

19.

Liu Y, Li T, Zhang C, Zhang W, Deng N, Dirk L . Raffinose positively regulates maize drought tolerance by reducing leaf transpiration. Plant J. 2023; 114(1):55-67. DOI: 10.1111/tpj.16116. View

20.

Sun X, Wang P, Jia X, Huo L, Che R, Ma F . Improvement of drought tolerance by overexpressing MdATG18a is mediated by modified antioxidant system and activated autophagy in transgenic apple. Plant Biotechnol J. 2017; 16(2):545-557. PMC: 5787838. DOI: 10.1111/pbi.12794. View