Abstract
Plants are exposed to various environmental cues that lead to reactive oxygen species (ROS) accumulation. ROS production and detoxification are tightly regulated to maintain balance. Although studies of glucose (Glc) are always accompanied by ROS in animals, the role of Glc in respect of ROS in plants is unclear. We isolated gsm2 (Glc-hypersensitive mutant 2), a mutant with a notably chlorotic-cotyledon phenotype. The chloroplast-localized GSM2 was characterized as a transaldolase in the pentose phosphate pathway. With 3% Glc treatment, fewer or no thylakoids were observed in gsm2 cotyledon chloroplasts than in wild-type cotyledon chloroplasts, suggesting that GSM2 is required for chloroplast protection under stress. gsm2 also showed evaluated accumulation of ROS with 3% Glc treatment and was more sensitive to exogenous H2O2 than the wild type. Gene expression analysis of the antioxidant enzymes in gsm2 revealed that chloroplast damage to gsm2 cotyledons results from the accumulation of excessive ROS in response to Glc. Moreover, the addition of diphenyleneiodonium chloride or phenylalanine can rescue Glc-induced chlorosis in gsm2 cotyledons. This work suggests that GSM2 functions to maintain ROS balance in response to Glc during early seedling growth and sheds light on the relationship between Glc, the pentose phosphate pathway and ROS.
Key message
The chloroplast-localized GSM2 is a transaldolase in the pentose phosphate pathway, which functions in the regulation of glucose-induced ROS to protect chloroplasts from oxidative damage during Arabidopsis early seedling growth.
Similar content being viewed by others
References
Avin-Wittenberg T (2019) Autophagy and its role in plant abiotic stress management. Plant Cell Environ 42:1045–1053
Bennett CF, Kwon JJ, Chen C, Russell J, Acosta K, Burnaevskiy N, Crane MM, Bitto A, Vander Wende H, Simko M, Pineda V, Rossner R, Wasko BM, Choi H, Chen S, Park S, Jafari G, Sands B, Perez Olsen C, Mendenhall AR, Morgan PG, Kaeberlein M (2017) Transaldolase inhibition impairs mitochondrial respiration and induces a starvation-like longevity response in Caenorhabditis elegans. PLoS Genet 13:e1006695
Caillau M, Paul Quick W (2005) New insights into plant transaldolase. Plant J 43:1–16
Carvalho RF, Szakonyi D, Simpson CG, Barbosa IC, Brown JW, Baena-Gonzalez E, Duque P (2016) The Arabidopsis SR45 splicing factor, a negative regulator of sugar signaling, modulates SNF1-related protein kinase 1 stability. Plant Cell 28:1910–1925
Ceusters J, Van de Poel B (2018) Ethylene exerts species-specific and age-dependent control of photosynthesis. Plant Physiol 176:2601–2612
Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743
Corbineau F, Xia Q, Bailly C, El-Maarouf-Bouteau H (2014) Ethylene, a key factor in the regulation of seed dormancy. Front Plant Sci 5:539
Couee I, Sulmon C, Gouesbet G, El Amrani A (2006) Involvement of soluble sugars in reactive oxygen species balance and responses to oxidative stress in plants. J Exp Bot 57:449–459
Czarnocka W, Karpinski S (2018) Friend or foe? Reactive oxygen species production, scavenging and signaling in plant response to environmental stresses. Free Radic Biol Med 122:4–20
Czechowski T, Stitt M, Altmann T, Udvardi MK, Scheible WR (2005) Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol 139:5–17
Daniell H, Lin CS, Yu M, Chang WJ (2016) Chloroplast genomes: diversity, evolution, and applications in genetic engineering. Genome Biol 17:134
Das K, Roychoudhury A (2014) Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants. Front Environ Sci. https://doi.org/10.3389/fenvs.2014.00053s
de Vries L, Vanholme R, Van Acker R, De Meester B, Sundin L, Boerjan W (2018) Stacking of a low-lignin trait with an increased guaiacyl and 5-hydroxyguaiacyl unit trait leads to additive and synergistic effects on saccharification efficiency in Arabidopsis thaliana. Biotechnol Biofuels 11:257
Dekkers BJ, Schuurmans JA, Smeekens SC (2008) Interaction between sugar and abscisic acid signalling during early seedling development in Arabidopsis. Plant Mol Biol 67:151–167
Demidchik V (2015) Mechanisms of oxidative stress in plants: from classical chemistry to cell biology. Environ Exp Bot 109:212–228
Dietz KJ, Turkan I, Krieger-Liszkay A (2016) Redox- and reactive oxygen species-dependent signaling into and out of the photosynthesizing chloroplast. Plant Physiol 171:1541–1550
Dong T, Park Y, Hwang I (2015) Abscisic acid: biosynthesis, inactivation, homoeostasis and signalling. Essays Biochem 58:29–48
Dong J, Sun N, Yang J, Deng Z, Lan J, Qin G, He H, Deng XW, Irish VF, Chen H, Wei N (2019) The transcription factors TCP4 and PIF3 antagonistically regulate organ-specific light induction of SAUR genes to modulate cotyledon opening during de-etiolation in arabidopsis. Plant Cell 5:1155–1170
Emiliani J, Grotewold E, Falcone Ferreyra ML, Casati P (2013) Flavonols protect Arabidopsis plants against UV-B deleterious effects. Mol Plant 6:1376–1379
Foyer CH, Noctor G (2005) Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell 17:1866–1875
Fu Y, Lim S, Urano D, Tunc-Ozdemir M, Phan NG, Elston TC, Jones AM (2014) Reciprocal encoding of signal intensity and duration in a glucose-sensing circuit. Cell 156:1084–1095
He J, Duan Y, Hua D, Fan G, Wang L, Liu Y, Chen Z, Han L, Qu LJ, Gong Z (2012) DEXH box RNA helicase-mediated mitochondrial reactive oxygen species production in Arabidopsis mediates crosstalk between abscisic acid and auxin signaling. Plant Cell 24:1815–1833
Holscher C, Meyer T, von Schaewen A (2014) Dual-targeting of Arabidopsis 6-phosphogluconolactonase 3 (PGL3) to chloroplasts and peroxisomes involves interaction with Trx m2 in the cytosol. Mol Plant 7:252–255
Hsiao YC, Hsu YF, Chen YC, Chang YL, Wang CS (2016) A WD40 protein, AtGHS40, negatively modulates abscisic acid degrading and signaling genes during seedling growth under high glucose conditions. J Plant Res 129:1127–1140
Hsu YF, Chen YC, Hsiao YC, Wang BJ, Lin SY, Cheng WH, Jauh GY, Harada JJ, Wang CS (2014) AtRH57, a DEAD-box RNA helicase, is involved in feedback inhibition of glucose-mediated abscisic acid accumulation during seedling development and additively affects pre-ribosomal RNA processing with high glucose. Plant J 77:119–135
Huang L, Yu LJ, Zhang X, Fan B, Wang FZ, Dai YS, Qi H, Zhou Y, Xie LJ, Xiao S (2019) Autophagy regulates glucose-mediated root meristem activity by modulating ROS production in Arabidopsis. Autophagy 15:407–422
Janse van Rensburg HC, Van den Ende W (2017) UDP-glucose: a potential signaling molecule in plants? Front Plant Sci 8:2230
Janse van Rensburg HC, Van den Ende W, Signorelli S (2019) Autophagy in plants: both a puppet and a puppet master of sugars. Front Plant Sci 10:14
Jarvis P, Lopez-Juez E (2013) Biogenesis and homeostasis of chloroplasts and other plastids. Nat Rev Mol Cell Biol 14:787–802
Keunen E, Peshev D, Vangronsveld J, Van Den Ende W, Cuypers A (2013) Plant sugars are crucial players in the oxidative challenge during abiotic stress: extending the traditional concept. Plant Cell Environ 36:1242–1255
Kleniewska P, Piechota A, Skibska B, Goraca A (2012) The NADPH oxidase family and its inhibitors. Arch Immunol Ther Exp (Warsz) 60:277–294
Kmiecik P, Leonardelli M, Teige M (2016) Novel connections in plant organellar signalling link different stress responses and signalling pathways. J Exp Bot 67:3793–3807
Kruger NJ, von Schaewen A (2003) The oxidative pentose phosphate pathway: structure and organisation. Curr Opin Plant Biol 6:236–246
Kumari P, Reddy CR, Jha B (2015) Methyl Jasmonate-induced lipidomic and biochemical alterations in the intertidal macroalga Gracilaria dura (Gracilariaceae, Rhodophyta). Plant Cell Physiol 56:1877–1889
León P (2003) Sugar and hormone connections. Trends Plant Sci 8:110–116
Leymarie J, Vitkauskaite G, Hoang HH, Gendreau E, Chazoule V, Meimoun P, Corbineau F, El-Maarouf-Bouteau H, Bailly C (2012) Role of reactive oxygen species in the regulation of Arabidopsis seed dormancy. Plant Cell Physiol 53:96–106
Li L, Sheen J (2016) Dynamic and diverse sugar signaling. Curr Opin Plant Biol 33:116–125
Li Y, Lee KK, Walsh S, Smith C, Hadingham S, Sorefan K, Cawley G, Bevan MW (2006) Establishing glucose- and ABA-regulated transcription networks in Arabidopsis by microarray analysis and promoter classification using a relevance vector machine. Genome Res 16:414–427
Liu Y, He J, Chen Z, Ren X, Hong X, Gong Z (2010) ABA overly-sensitive 5 (ABO5), encoding a pentatricopeptide repeat protein required for cis-splicing of mitochondrial nad2 intron 3, is involved in the abscisic acid response in Arabidopsis. Plant J 63:749–765
Luo J, Xiang Y, Xu X, Fang D, Li D, Ni F, Zhu X, Chen B, Zhou M (2018) High glucose-induced ROS production stimulates proliferation of pancreatic cancer via inactivating the JNK pathway. Oxid Med Cell Longev 2018:6917206
Maeda H, Dudareva N (2012) The shikimate pathway and aromatic amino acid biosynthesis in plants. Annu Rev Plant Biol 63:73–105
Maloney GS, DiNapoli KT, Muday GK (2014) The anthocyanin reduced tomato mutant demonstrates the role of flavonols in tomato lateral root and root hair development. Plant Physiol 166:614–631
Mhamdi A, Van Breusegem F (2018) Reactive oxygen species in plant development. Development 145:dev164376
Mira M, Hill RD, Stasolla C (2016) Regulation of programmed cell death by phytoglobins. J Exp Bot 67:5901–5908
Mittler R (2017) ROS are good. Trends Plant Sci 22:11–19
Mittler R, Blumwald E (2015) The roles of ROS and ABA in systemic acquired acclimation. Plant Cell 27:64–70
Moehs CP, Allen PV, Friedman M, Belknap WR (1996) Cloning and expression of transaldolase from potato. Plant Mol Biol 32:447–452
Moore B, Zhou L, Rolland F, Hall Q, Cheng WH, Liu YX, Hwang I, Jones T, Sheen J (2003) Role of the Arabidopsis glucose sensor HXK1 in nutrient, light, and hormonal signaling. Science 300:332–336
Muhlemann JK, Younts TLB, Muday GK (2018) Flavonols control pollen tube growth and integrity by regulating ROS homeostasis during high-temperature stress. Proc Natl Acad Sci USA 115:E11188–E11197
Overmyer K, Brosché M, Kangasjärvi J (2003) Reactive oxygen species and hormonal control of cell death. Trends Plant Sci 8:335–342
Para A, Muhammad D, Orozco-Nunnelly DA, Memishi R, Alvarez S, Naldrett MJ, Warpeha KM (2016) The dehydratase ADT3 Affects ROS homeostasis and cotyledon development. Plant Physiol 172:1045–1060
Parthasarathy A, Cross PJ, Dobson RCJ, Adams LE, Savka MA, Hudson AO (2018) A three-ring circus: metabolism of the three proteogenic aromatic amino acids and their role in the health of plants and animals. Front Mol Biosci 5:29
Perl A, Qian Y, Chohan KR, Shirley CR, Amidon W, Banerjee S, Middleton FA, Conkrite KL, Barcza M, Gonchoroff N, Suarez SS, Banki K (2006) Transaldolase is essential for maintenance of the mitochondrial transmembrane potential and fertility of spermatozoa. Proc Natl Acad Sci USA 103:14813–14818
Perl A, Hanczko R, Telarico T, Oaks Z, Landas S (2011) Oxidative stress, inflammation and carcinogenesis are controlled through the pentose phosphate pathway by transaldolase. Trends Mol Med 17:395–403
Pogson BJ, Albrecht V (2011) Genetic dissection of chloroplast biogenesis and development: an overview. Plant Physiol 155:1545–1551
Porra RJ (2002) The chequered history of the development and use of simultaneous equations for the accurate determination of chlorophylls a and b. Photosynth Res 73:149–156
Qi J, Wang J, Gong Z, Zhou JM (2017) Apoplastic ROS signaling in plant immunity. Curr Opin Plant Biol 38:92–100
Qian Y, Banerjee S, Grossman CE, Amidon W, Nagy G, Barcza M, Niland B, Karp DR, Middleton FA, Banki K, Perl A (2008) Transaldolase deficiency influences the pentose phosphate pathway, mitochondrial homoeostasis and apoptosis signal processing. Biochem J 415:123–134
Raja V, Majeed U, Kang H, Andrabi KI, John R (2017) Abiotic stress: interplay between ROS, hormones and MAPKs. Environ Exp Bot 137:142–157
Rodrigues A, Adamo M, Crozet P, Margalha L, Confraria A, Martinho C, Elias A, Rabissi A, Lumbreras V, Gonzalez-Guzman M, Antoni R, Rodriguez PL, Baena-Gonzalez E (2013) ABI1 and PP2CA phosphatases are negative regulators of Snf1-related protein kinase1 signaling in Arabidopsis. Plant Cell 25:3871–3884
Rolland N, Curien G, Finazzi G, Kuntz M, Marechal E, Matringe M, Ravanel S, Seigneurin-Berny D (2012) The biosynthetic capacities of the plastids and integration between cytoplasmic and chloroplast processes. Annu Rev Genet 46:233–264
Sakr S, Wang M, Dedaldechamp F, Perez-Garcia MD, Oge L, Hamama L, Atanassova R (2018) The sugar-signaling hub: overview of regulators and interaction with the hormonal and metabolic network. Int J Mol Sci 19:2506
Schulz TJ, Zarse K, Voigt A, Urban N, Birringer M, Ristow M (2007) Glucose restriction extends Caenorhabditis elegans life span by inducing mitochondrial respiration and increasing oxidative stress. Cell Metab 6:280–293
Semenza GL (2017) Hypoxia-inducible factors: coupling glucose metabolism and redox regulation with induction of the breast cancer stem cell phenotype. EMBO J 36:252–259
Shah MS, Brownlee M (2016) Molecular and cellular mechanisms of cardiovascular disorders in diabetes. Circ Res 118:1808–1829
Sheen J (2014) Master regulators in plant glucose signaling networks. J Plant Biol 57:67–79
Shigeoka S, Maruta T (2014) Cellular redox regulation, signaling, and stress response in plants. Biosci Biotechnol Biochem 78:1457–1470
Shimada H, Mochizuki M, Ogura K, Froehlich JE, Osteryoung KW, Shirano Y, Shibata D, Masuda S, Mori K, Takamiya K (2007) Arabidopsis cotyledon-specific chloroplast biogenesis factor CYO1 is a protein disulfide isomerase. Plant Cell 19:3157–3169
Signorelli S, Tarkowski LP, Van den Ende W, Bassham DC (2019) Linking autophagy to abiotic and biotic stress responses. Trends Plant Sci 24:413–430
Singh R, Parihar P, Singh S, Mishra RK, Singh VP, Prasad SM (2017) Reactive oxygen species signaling and stomatal movement: current updates and future perspectives. Redox Biol 11:213–218
Stincone A, Prigione A, Cramer T, Wamelink MM, Campbell K, Cheung E, Olin-Sandoval V, Gruning NM, Kruger A, Tauqeer Alam M, Keller MA, Breitenbach M, Brindle KM, Rabinowitz JD, Ralser M (2015) The return of metabolism: biochemistry and physiology of the pentose phosphate pathway. Biol Rev Camb Philos Soc 90:927–963
Suzuki N, Katano K (2018) Coordination between ROS regulatory systems and other pathways under heat stress and pathogen attack. Front Plant Sci 9:490
Tanaka T, Tanaka H, Machida C, Watanabe M, Machida Y (2004) A new method for rapid visualization of defects in leaf cuticle reveals five intrinsic patterns of surface defects in Arabidopsis. Plant J 37:139–146
Tsukagoshi H (2016) Control of root growth and development by reactive oxygen species. Curr Opin Plant Biol 29:57–63
Van Aken O, Zhang B, Law S, Narsai R, Whelan J (2013) AtWRKY40 and AtWRKY63 modulate the expression of stress-responsive nuclear genes encoding mitochondrial and chloroplast proteins. Plant Physiol 162:254–271
Vanholme R, Storme V, Vanholme B, Sundin L, Christensen JH, Goeminne G, Halpin C, Rohde A, Morreel K, Boerjan W (2012) A systems biology view of responses to lignin biosynthesis perturbations in Arabidopsis. Plant Cell 24:3506–3529
Wang S, Moustaid-Moussa N, Chen L, Mo H, Shastri A, Su R, Bapat P, Kwun I, Shen CL (2014) Novel insights of dietary polyphenols and obesity. J Nutr Biochem 25:1–18
Waszczak C, Carmody M, Kangasjarvi J (2018) Reactive oxygen species in plant signaling. Annu Rev Plant Biol 69:209–236
Watkins JM, Chapman JM, Muday GK (2017) Abscisic acid-induced reactive oxygen species are modulated by flavonols to control stomata aperture. Plant Physiol 175:1807–1825
Wu W, Yan Y (2018) Chloroplast proteome analysis of Nicotiana tabacum overexpressing TERF1 under drought stress condition. Bot Stud 59:26
Xiao G, Zhou J, Lu X, Huang R, Zhang H (2018) Excessive UDPG resulting from the mutation of UAP1 causes programmed cell death by triggering reactive oxygen species accumulation and caspase-like activity in rice. New Phytol 217:332–343
Xu Z, Rothstein SJ (2018) ROS-Induced anthocyanin production provides feedback protection by scavenging ROS and maintaining photosynthetic capacity in Arabidopsis. Plant Signal Behav 13:e1451708
Yang L, Zhang J, He J, Qin Y, Hua D, Duan Y, Chen Z, Gong Z (2014) ABA-mediated ROS in mitochondria regulate root meristem activity by controlling PLETHORA expression in Arabidopsis. PLoS Genet 10:e1004791
Yang Z, Zhou Y, Huang J, Hu Y, Zhang E, Xie Z, Ma S, Gao Y, Song S, Xu C, Liang G (2015) Ancient horizontal transfer of transaldolase-like protein gene and its role in plant vascular development. New Phytol 206:807–816
Yoo SD, Cho YH, Sheen J (2007) Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat Protoc 2:1565–1572
Zheng M, Yang T, Tao P, Zhu C, Fu Y, Hsu YF (2019) Arabidopsis GSM1 is involved in ABI4-regulated ABA signaling under high-glucose condition in early seedling growth. Plant Sci 287:110183
Zipfel C (2013) Combined roles of ethylene and endogenous peptides in regulating plant immunity and growth. Proc Natl Acad Sci USA 110:5748–5749
Acknowledgements
This work was supported by the National Natural Science Foundation of China (31600987) and the Program for Innovation Team Building at Institution of Higher Education in Chongqing (CXTDX201601009).
Author information
Authors and Affiliations
Contributions
Y-FH and MZ designed the research. MZ, CZ, TY and JQ performed the experiments. MZ, CZ and Y-FH analyzed the data. MZ and Y-FH wrote the manuscript. All authors read and approved the manuscript. MZ and CZ contributed equally to this work.
Corresponding author
Ethics declarations
Conflict of interest
The authors have no conflicts of interest to declare.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Zheng, M., Zhu, C., Yang, T. et al. GSM2, a transaldolase, contributes to reactive oxygen species homeostasis in Arabidopsis. Plant Mol Biol 104, 39–53 (2020). https://doi.org/10.1007/s11103-020-01022-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11103-020-01022-x