Investigating the effect of drought stress and methanol spraying on the influential genes in the Calvin cycle and photorespiration of rapeseed (Brassica napus)
Parisa Taghvimi A , Mohammad Mohsenzadeh Golfazani
A * , Mohammad Mahdi Taghvaei A and Habibollah Samizadeh Lahiji A
A
Abstract
Due to global warming and changes in precipitation patterns, many regions are prone to permanent drought. Rapeseed (Brassica napus) is one of the main sources of edible oils worldwide, and its production and yield are affected by drought. In this study, gene expression alterations under drought stress are investigated with bioinformatics studies to examine evolutionary relations of conserved motifs structure and interactions among Calvin cycle and photorespiration pathways key genes in drought-tolerant (SLM046) and drought-sensitive (Hayola308) genotypes of rapeseed. Investigating the conservation and evolutionary relationships revealed high conservation in motifs of FBPase, PRK, GlyK and NADP-ME enzymes. The analysis of protein interactions showed the correlation between FTRC, FBPase1, PRKX1, GlyKX2 and NADP-ME4 genes. Furthermore, in rapeseed, for the GlyKX2 and NADP-ME4 genes, four microRNAs of the miR172 family and four members of the miR167 family were identified as post-transcriptional regulators, respectively. The expression of ferredoxin thioredoxin reductase, fructose-1,6-bisphosphatase genes, phosphoribulokinase, glycerate kinase and malic enzyme 4 genes in the two rapeseed genotypes were evaluated by real-time qPCR method under 72 h of drought stress and methanol foliar application. As a result, the highest expression levels of FTRC, PRKX1, GlyKX2, NADP-ME4 and FBPase1 were observed in methanol foliar application on the SLM046 genotype at 24 h. In contrast, in methanol foliar application on the Hayola308 genotype, the highest expression levels of FTRC, PRKX1, GlyKX2, NADP-ME4 and FBPase1 were observed 8 h after the treatment. Our study illustrated that methanol foliar application enhanced plant tolerance under drought stress.
Keywords: abiotic stress, bioinformatics, Brassicaceae, Calvin cycle, conserved motifs, drought stress, microRNAs, photorespiration, protein interactions.
References
Abebe T, Wise RP, Skadsen RW (2009) Comparative transcriptional profiling established the awn as the major photosynthetic organ of the barley spike while the lemma and the palea primarily protect the seed. The Plant Genome 2, 247-259.
| Crossref | Google Scholar |
Ali S, Hayat K, Iqbal A, Xie L (2020) Implications of abscisic acid in the drought stress tolerance of plants. Agronomy 10, 1323.
| Crossref | Google Scholar |
Andres AR, Lazaro JJ, Chueca A, Hermoso R, Gorge JL (1990) Effect of alcohols on the association of photosynthetic fructose-1,6-bisphosphatase to thylakoid membranes. Physiologia Plantarum 78, 409-413.
| Crossref | Google Scholar |
Arias CL, Pavlovic T, Torcolese G, Badia MB, Gismondi M, Maurino VG, Andreo CS, Drincovich MF, Gerrard Wheeler MC, Saigo M (2018) NADP-dependent malic enzyme 1 participates in the abscisic acid response in Arabidopsis thaliana. Frontiers in Plant Science 9, 1-11.
| Crossref | Google Scholar |
Aryal UK, Xiong Y, McBride Z, Kihara D, Xie J, Hall MC, Szymanski DB (2014) A proteomic strategy for global analysis of plant protein complexes. The Plant Cell 26, 3867-3882.
| Crossref | Google Scholar | PubMed |
Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116, 281-297.
| Crossref | Google Scholar | PubMed |
Bhardwaj AR, Joshi G, Pandey R, Kukreja B, Goel S, Jagannath A, Kumar A, Katiyar-Agarwal S, Agarwal M (2014) A genome-wide perspective of miRNAome in response to high temperature, salinity and drought stresses in Brassica juncea (Czern) L. PLoS ONE 9, e92456.
| Crossref | Google Scholar | PubMed |
Biehler K, Fock H (1996) Evidence for the contribution of the Mehler-peroxidase reaction in dissipating excess electrons in drought-stressed wheat. Plant Physiology 112, 265-272.
| Crossref | Google Scholar | PubMed |
Bloom AJ, Lancaster KM (2018) Manganese binding to Rubisco could drive a photorespiratory pathway that increases the energy efficiency of photosynthesis. Nature Plants 4, 414-422.
| Crossref | Google Scholar | PubMed |
Boldt R, Edner C, Kolukisaoglu Ü, Hagemann M, Weckwerth W, Wienkoop S, Morgenthal K, Bauwe H (2005) D-GLYCERATE3-KINASE, the last unknown enzyme in the photorespiratory cycle in Arabidopsis, belongs to a novel kinase family. The Plant Cell 17, 2413-2420.
| Crossref | Google Scholar | PubMed |
Brandes HK, Hartman FC, Lu T-YS, Larimer FW (1996) Efficient expression of the gene for spinach phosphoribulokinase in Pichia pastoris and utilization of the recombinant enzyme to explore the role of regulatory cysteinyl residues by site-directed mutagenesis. Journal of Biological Chemistry 271, 6490-6496.
| Crossref | Google Scholar | PubMed |
Chaves MM (1991) Effects of water deficits on carbon assimilation. Journal of Experimental Botany 42, 1-16.
| Crossref | Google Scholar |
Chen Q, Wang B, Ding H, Zhang J, Li S (2019) Review: the role of NADP-malic enzyme in plants under stress. Plant Science 281, 206-212.
| Crossref | Google Scholar | PubMed |
Cheng Y, Zhan H, Yang W, Jiang Q, Wang Y, Guo F (2021) An ecohydrological perspective of reconstructed vegetation in the semi-arid region in drought seasons. Agricultural Water Management 243, 106488.
| Crossref | Google Scholar |
Covarrubias AA, Reyes JL (2010) Post-transcriptional gene regulation of salinity and drought responses by plant microRNAs. Plant, Cell & Environment 33, 481-489.
| Crossref | Google Scholar | PubMed |
Dai S, Schwendtmayer C, Johansson K, Ramaswamy S, Schürmann P, Eklund H (2000) How does light regulate chloroplast enzymes? Structure–function studies of the ferredoxin/thioredoxin system. Quarterly Reviews of Biophysics 33, 67-108.
| Crossref | Google Scholar | PubMed |
Dai X, Zhuang Z, Zhao PX (2018) psRNATarget: a plant small RNA target analysis server (2017 release). Nucleic Acids Research 46, W49-W54.
| Crossref | Google Scholar |
Deeba F, Pandey AK, Ranjan S, Mishra A, Singh R, Sharma YK, Shirke PA, Pandey V (2012) Physiological and proteomic responses of cotton (Gossypium herbaceum L.) to drought stress. Plant Physiology and Biochemistry 53, 6-18.
| Crossref | Google Scholar | PubMed |
Dias MC, Brüggemann W (2010) Limitations of photosynthesis in Phaseolus vulgaris under drought stress: gas exchange, chlorophyll fluorescence and Calvin cycle enzymes. Photosynthetica 48, 96-102.
| Crossref | Google Scholar |
Doubnerová Hýsková V, Miedzińska L, Dobrá J, Vankova R, Ryšlavá H (2014) Phosphoenolpyruvate carboxylase, NADP-malic enzyme, and pyruvate, phosphate dikinase are involved in the acclimation of Nicotiana tabacum L. to drought stress. Journal of Plant Physiology 171, 19-25.
| Crossref | Google Scholar |
Downie A, Miyazaki S, Bohnert H, John P, Coleman J, Parry M, Haslam R (2004) Expression profiling of the response of Arabidopsis thaliana to methanol stimulation. Phytochemistry 65, 2305-2316.
| Crossref | Google Scholar |
Farooq M, Wahid A, Kobayashi N, Fujita D, Basra SMA (2009) Plant drought stress: effects, mechanisms and management. In ‘Sustainable agriculture’. (Eds E Lichtfouse, M Navarrete, P Debaeke, S Véronique, C Alberola) pp. 153–188. (Springer) doi:10.1051/agro:2008021
Farooq MS, Uzair M, Raza A, Habib M, Xu Y, Yousuf M, Yang SH, Ramzan Khan M (2022) Uncovering the research gaps to alleviate the negative impacts of climate change on food security: a review. Frontiers in Plant Science 13, 927535.
| Crossref | Google Scholar |
Fu J, Huang B (2001) Involvement of antioxidants and lipid peroxidation in the adaptation of two cool-season grasses to localized drought stress. Environmental and Experimental Botany 45, 105-114.
| Crossref | Google Scholar | PubMed |
Gout E, Aubert S, Bligny R, Rébeillé F, Nonomura AR, Benson AA, Douce R (2000) Metabolism of methanol in plant cells. Carbon-13 nuclear magnetic resonance studies. Plant Physiology 123, 287-296.
| Crossref | Google Scholar | PubMed |
Guo R, Deng Y, Huang Z, Chen X, XuHan X, Lai Z (2016) Identification of miRNAs affecting the establishment of Brassica Alboglabra seedling. Frontiers in Plant Science 7, 1760.
| Crossref | Google Scholar | PubMed |
Han Y, Zhang X, Wang Y, Ming F (2013) The suppression of WRKY44 by GIGANTEA-miR172 pathway is involved in drought response of Arabidopsis thaliana. PLoS ONE 8, e73541.
| Crossref | Google Scholar | PubMed |
Hanson AD, Roje S (2001) One-carbon metabolism in higher plants. Annual Review of Plant Physiology and Plant Molecular Biology 52, 119-137.
| Crossref | Google Scholar | PubMed |
Hebbelmann I, Selinski J, Wehmeyer C, Goss T, Voss I, Mulo P, Kangasjärvi S, Aro E-M, Oelze M-L, Dietz K-J, Nunes-Nesi A, Do PT, Fernie AR, Talla SK, Raghavendra AS, Linke V, Scheibe R (2012) Multiple strategies to prevent oxidative stress in Arabidopsis plants lacking the malate valve enzyme NADP-malate dehydrogenase. Journal of Experimental Botany 63, 1445-1459.
| Crossref | Google Scholar | PubMed |
Hishiya S, Hatakeyama W, Mizota Y, Hosoya-Matsuda N, Motohashi K, Ikeuchi M, Hisabori T (2008) Binary reducing equivalent pathways using NADPH-thioredoxin reductase and ferredoxin-thioredoxin reductase in the cyanobacterium Synechocystis sp. strain PCC 6803. Plant and Cell Physiology 49, 11-18.
| Crossref | Google Scholar | PubMed |
Jacquot J-P, Vidal J, Gadal P, Schürmann P (1978) Evidence for the existence of several enzyme-specific thioredoxins in plants. FEBS Letters 96, 243-246.
| Crossref | Google Scholar |
Keryer E, Collin V, Lavergne D, Lemaire S, Issakidis-Bourguet E (2004) Characterization of Arabidopsis mutants for the variable subunit of ferredoxin:thioredoxin reductase. Photosynthesis Research 79, 265-274.
| Crossref | Google Scholar | PubMed |
Khodadadi E, Fakheri BA, Aharizad S, Emamjomeh A, Norouzi M, Komatsu S (2017) Leaf proteomics of drought-sensitive and -tolerant genotypes of fennel. Biochimica et Biophysica Acta (BBA) – Proteins and Proteomics 1865, 1433-1444.
| Crossref | Google Scholar | PubMed |
Kim BH, Kwon Y, Lee B-H, Nam KH (2014) Overexpression of miR172 suppresses the brassinosteroid signaling defects of bak1 in Arabidopsis. Biochemical and Biophysical Research Communications 447, 479-484.
| Crossref | Google Scholar | PubMed |
Koh J, Chen G, Yoo M-J, Zhu N, Dufresne D, Erickson JE, Shao H, Chen S (2015) Comparative proteomic analysis of Brassica napus in response to drought stress. Journal of Proteome Research 14, 3068-3081.
| Crossref | Google Scholar | PubMed |
Koßmann J, Sonnewald U, Willmitzer L (1994) Reduction of the chloroplastic fructose-1,6-bisphosphatase in transgenic potato plants impairs photosynthesis and plant growth. The Plant Journal 6, 637-650.
| Crossref | Google Scholar |
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution 35, 1547.
| Crossref | Google Scholar | PubMed |
Li M, Yang Y, Raza A, Yin S, Wang H, Zhang Y, Dong J, Wang G, Zhong C, Zhang H, Liu J, Jin W (2021) Heterologous expression of Arabidopsis thaliana rty gene in strawberry (Fragaria × ananassa Duch.) improves drought tolerance. BMC Plant Biology 21, 57.
| Crossref | Google Scholar | PubMed |
Liang C, Wang W, Ma J, Wang J, Zhou F, Li W, Yu Y, Zhang L, Huang W, Huang X (2020) Identification of differentially expressed microRNAs of sunflower seedlings under drought stress. Agronomy Journal 112, 2472-2484.
| Crossref | Google Scholar |
Lim CJ, Kim WB, Lee B-S, Lee HY, Kwon T-H, Park JM, Kwon S-Y (2010) Silencing of SlFTR-c, the catalytic subunit of ferredoxin:thioredoxin reductase, induces pathogenesis-related genes and pathogen resistance in tomato plants. Biochemical and Biophysical Research Communications 399, 750-754.
| Crossref | Google Scholar | PubMed |
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25, 402-408.
| Crossref | Google Scholar | PubMed |
Lu K, Wei L, Li X, Wang Y, Wu J, Liu M, Zhang C, Chen Z, Xiao Z, Jian H, et al. (2019) Whole-genome resequencing reveals Brassica napus origin and genetic loci involved in its improvement. Nature Communications 10, 1154.
| Crossref | Google Scholar |
Maier A, Fahnenstich H, von Caemmerer S, Engqvist MKM, Weber APM, Flügge U-I, Maurino VG (2012) Transgenic introduction of a glycolate oxidative cycle into A. thaliana chloroplasts leads to growth improvement. Frontiers in Plant Science 3, 38.
| Crossref | Google Scholar | PubMed |
Marri L, Zaffagnini M, Collin V, Issakidis-Bourguet E, Lemaire SD, Pupillo P, Sparla F, Miginiac-Maslow M, Trost P (2009) Prompt and easy activation by specific thioredoxins of Calvin cycle enzymes of Arabidopsis thaliana associated in the GAPDH/CP12/PRK supramolecular complex. Molecular Plant 2, 259-269.
| Crossref | Google Scholar | PubMed |
Michelet L, Zaffagnini M, Morisse S, Sparla F, Pérez-Pérez ME, Francia F, Danon A, Marchand CH, Fermani S, Trost P, Lemaire SD (2013) Redox regulation of the Calvin–Benson cycle: something old, something new. Frontiers in Plant Science 4, 470.
| Crossref | Google Scholar | PubMed |
Mirzai M, Moeini A, Ghanati F (2013) Effects of drought stress on the lipid peroxidation and antioxidant enzyme activities in two canola (Brassica napus L.) cultivars. Journal of Agricultural Science and Technology 15, 593-602.
| Google Scholar |
Mohsenzadeh Golfazani M, Taghvaei MM, Samizadeh Lahiji H, Ashery S, Raza A (2022) Investigation of proteins’ interaction network and the expression pattern of genes involved in the ABA biogenesis and antioxidant system under methanol spray in drought-stressed rapeseed. 3 Biotech 12, 217.
| Crossref | Google Scholar | PubMed |
Nagaharu U, Nagaharu N (1935) Genome analysis in Brassica with special reference to the experimental formation of B. napus and peculiar mode of fertilization. Japanese Journal of Botany 7, 389-452.
| Google Scholar |
Nonomura A, Benson A (1992) The path of carbon in photosynthesis: improved crop yields with methanol. Proceedings of the National Academy of Sciences 89, 9794-9798.
| Crossref | Google Scholar |
Penfield S, Clements S, Bailey KJ, Gilday AD, Leegood RC, Gray JE, Graham IA (2012) Expression and manipulation of PHOSPHOENOLPYRUVATE CARBOXYKINASE 1 identifies a role for malate metabolism in stomatal closure. The Plant Journal 69, 679-688.
| Crossref | Google Scholar | PubMed |
Rahman MA, Woo JH, Song Y, Lee S-H, Hasan MM, Azad MAK, Lee K-W (2022) Heat shock proteins and antioxidant genes involved in heat combined with drought stress responses in perennial rye grass. Life 12, 1426.
| Crossref | Google Scholar | PubMed |
Ramezanzadeh Bishegahi S, Mohsenzadeh M, Samizadeh H (2021) Effect of methanol foliar application on expression changes of some mitochondrial genes in canola under drought stress. Iranian Journal of Field Crop Science 52, 113-128.
| Crossref | Google Scholar |
Ramírez I, Dorta F, Espinoza V, Jiménez E, Mercado A, Peña-Cortés H (2006) Effects of foliar and root applications of methanol on the growth of Arabidopsis, tobacco, and tomato plants. Journal of Plant Growth Regulation 25, 30-44.
| Crossref | Google Scholar |
Raza A, Su W, Gao A, Mehmood SS, Hussain MA, Nie W, Lv Y, Zou X, Zhang X (2021) Catalase (CAT) gene family in rapeseed (Brassica napus L.): genome-wide analysis, identification, and expression pattern in response to multiple hormones and abiotic stress conditions. International Journal of Molecular Sciences 22, 4281.
| Crossref | Google Scholar | PubMed |
Safarzadeh Vishekaei MN, Normohammadi G, Majidi-Haravan E, Rabiei B (2007) Effect of methanol on growth and yield of peanut (Arachis hypogaea L.). Agricultural Sciences 13, 87104.
| Google Scholar |
Schürmann P, Buchanan BB (2001) The structure and function of the ferredoxin/thioredoxin system in photosynthesis. In ‘Regulation of photosynthesis’. (Eds EM Aro, B Andersson) pp. 331–361. (Springer) doi:10.1007/0-306-48148-0_20
Schürmann P, Buchanan BB (2008) The ferredoxin/thioredoxin system of oxygenic photosynthesis. Antioxidants & Redox Signaling 10, 1235-1274.
| Crossref | Google Scholar | PubMed |
Schürmann P, Jacquot J-P (2000) Plant thioredoxin systems revisited. Annual Review of Plant Physiology and Plant Molecular Biology 51, 371-400.
| Crossref | Google Scholar | PubMed |
Secchi MA, Fernandez JA, Stamm MJ, Durrett T, Prasad PVV, Messina CD, Ciampitti IA (2023) Effects of heat and drought on canola (Brassica napus L.) yield, oil, and protein: a meta-analysis. Field Crops Research 293, 108848.
| Crossref | Google Scholar |
Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Research 13, 2498-2504.
| Crossref | Google Scholar | PubMed |
Shavrukov Y, Kurishbayev A, Jatayev S, Shvidchenko V, Zotova L, Koekemoer F, De Groot S, Soole K, Langridge P (2017) Early flowering as a drought escape mechanism in plants: how can it aid wheat production? Frontiers in Plant Science 8, 1950.
| Crossref | Google Scholar | PubMed |
Shi H, Ye T, Chan Z (2014) Comparative proteomic responses of two bermudagrass (Cynodon dactylon (L). Pers.) varieties contrasting in drought stress resistance. Plant Physiology and Biochemistry 82, 218-228.
| Crossref | Google Scholar | PubMed |
Shivaraj SM, Dhakate P, Mayee P, Negi MS, Singh A (2014) Natural genetic variation in MIR172 isolated from Brassica species. Biologia Plantarum 58, 627-640.
| Crossref | Google Scholar |
Sun X, Han G, Meng Z, Lin L, Sui N (2019) Roles of malic enzymes in plant development and stress responses. Plant Signaling & Behavior 14, e1644596.
| Crossref | Google Scholar | PubMed |
Szklarczyk D, Gable AL, Lyon D, Junge A, Wyder S, Huerta-Cepas J, Simonovic M, Doncheva NT, Morris JH, Bork P, Jensen LJ, Mering Cv (2019) STRING v11: protein–protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets. Nucleic Acids Research 47, D607-D613.
| Crossref | Google Scholar | PubMed |
Tabita FR (1994) The biochemistry and molecular regulation of carbon dioxide metabolism in cyanobacteria. In ‘The molecular biology of cyanobacteria’. (Ed. DA Bryant) pp. 437–467. (Springer) doi:10.1007/978-94-011-0227-8_14
Taghvaei MM, Samizadeh Lahiji H, Bakhtiarizadeh MR, Mohsenzadeh Golafazani M (2019) Bioinformatics analysis of microRNAs related to cold stress and their effects on proteins associated with fatty acids metabolism in rapeseed (Brassica napus L.). Crop Biotechnology 9, 41-58.
| Crossref | Google Scholar |
Taghvaei MM, Lahiji HS, Golfazani MM (2022) Evaluation of expression changes, proteins interaction network, and microRNAs targeting catalase and superoxide dismutase genes under cold stress in rapeseed (Brassica napus L.). OCL 29, 3.
| Crossref | Google Scholar |
Tran D, Dauphin A, Meimoun P, Kadono T, Nguyen HTH, Arbelet-Bonnin D, Zhao T, Errakhi R, Lehner A, Kawano T, Bouteau F (2018) Methanol induces cytosolic calcium variations, membrane depolarization and ethylene production in Arabidopsis and tobacco. Annals of Botany 122, 849-860.
| Crossref | Google Scholar | PubMed |
Tran MT, Doan DTH, Kim J, Song YJ, Sung YW, Das S, Kim E-J, Son GH, Kim SH, Van Vu T, Kim J-Y (2021) CRISPR/Cas9-based precise excision of SlHyPRP1 domain(s) to obtain salt stress-tolerant tomato. Plant Cell Reports 40, 999-1011.
| Crossref | Google Scholar | PubMed |
Varshney RK, Barmukh R, Roorkiwal M, Qi Y, Kholova J, Tuberosa R, Reynolds MP, Tardieu F, Siddique KHM (2021) Breeding custom-designed crops for improved drought adaptation. Advanced Genetics 2, e202100017.
| Crossref | Google Scholar |
Vieira Dos Santos C, Cuiné S, Rouhier N, Rey P (2005) The Arabidopsis plastidic methionine sulfoxide reductase B proteins. Sequence and activity characteristics, comparison of the expression with plastidic methionine sulfoxide reductase A, and induction by photooxidative stress. Plant Physiology 138, 909-922.
| Crossref | Google Scholar | PubMed |
Walters EM, Garcia-Serres R, Jameson GNL, Glauser DA, Bourquin F, Manieri W, Schürmann P, Johnson MK, Huynh BH (2005) Spectroscopic characterization of site-specific [Fe4S4] cluster chemistry in ferredoxin:thioredoxin reductase: implications for the catalytic mechanism. Journal of the American Chemical Society 127, 9612-9624.
| Crossref | Google Scholar | PubMed |
Walters EM, Garcia-Serres R, Naik SG, Bourquin F, Glauser DA, Schürmann P, Huynh BH, Johnson MK (2009) Role of histidine-86 in the catalytic mechanism of ferredoxin: thioredoxin reductase. Biochemistry 48, 1016-1024.
| Crossref | Google Scholar | PubMed |
Wang P, Liu J, Liu B, Da Q, Feng D, Su J, Zhang Y, Wang J, Wang H-B (2014) Ferredoxin:thioredoxin reductase is required for proper chloroplast development and is involved in the regulation of plastid gene expression in Arabidopsis thaliana. Molecular Plant 7, 1586-1590.
| Crossref | Google Scholar | PubMed |
Wang G, Tian C, Wang Y, Wan F, Hu L, Xiong A, Tian J (2019) Selection of reliable reference genes for quantitative RT-PCR in garlic under salt stress. PeerJ 7, e7319.
| Crossref | Google Scholar | PubMed |
Wasaya A, Manzoor S, Yasir TA, Sarwar N, Mubeen K, Ismail IA, Raza A, Rehman A, Hossain A, El Sabagh A (2021) Evaluation of fourteen bread wheat (Triticum aestivum L.) genotypes by observing gas exchange parameters, relative water and chlorophyll content, and yield attributes under drought stress. Sustainability 13, 4799.
| Crossref | Google Scholar |
Wen Z, Wang Y, Xia C, Zhang Y, Zhang H (2021) Chloroplastic SaNADP-ME4 of C3–C4 woody desert species Salsola laricifolia confers drought and salt stress resistance to Arabidopsis. Plants 10, 1827.
| Crossref | Google Scholar | PubMed |
Wingler A, Quick WP, Bungard RA, Bailey KJ, Lea PJ, Leegood RC (1999) The role of photorespiration during drought stress: an analysis utilizing barley mutants with reduced activities of photorespiratory enzymes. Plant, Cell & Environment 22, 361-373.
| Crossref | Google Scholar |
Yao X, Chen J, Zhou J, Yu H, Ge C, Zhang M, Gao X, Dai X, Yang Z-N, Zhao Y (2019) An essential role for miRNA167 in maternal control of embryonic and seed development. Plant Physiology 180, 453-464.
| Crossref | Google Scholar | PubMed |
Zbieć I, Karczmarczyk S, Podsiadło C (2003) Response of some cultivated plants to methanol as compared to supplemental irrigation. Electronic Journal of Polish Agricultural Universities 6, 1-7.
| Google Scholar |
Zhang C, Zhang L, Zhang S, Zhu S, Wu P, Chen Y, Li M, Jiang H, Wu G (2015) Global analysis of gene expression profiles in physic nut (Jatropha curcas L.) seedlings exposed to drought stress. BMC Plant Biology 15, 17.
| Crossref | Google Scholar |
Zybailov B, Rutschow H, Friso G, Rudella A, Emanuelsson O, Sun Q, van Wijk KJ (2008) Sorting signals, N-terminal modifications and abundance of the chloroplast proteome. PLoS ONE 3, e1994.
| Crossref | Google Scholar | PubMed |
