Physiological and biochemical responses of soybean plants inoculated with Arbuscular mycorrhizal fungi and Bradyrhizobium under drought stress

. 2021 Apr 22 ; 21 (1) : 195. [epub] 20210422

Jazyk angličtina Země Velká Británie, Anglie Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid33888066
Odkazy

PubMed 33888066
PubMed Central PMC8061216
DOI 10.1186/s12870-021-02949-z
PII: 10.1186/s12870-021-02949-z
Knihovny.cz E-zdroje

BACKGROUND: The present study aims to study the effects of biofertilizers potential of Arbuscular Mycorrhizal Fungi (AMF) and Bradyrhizobium japonicum (B. japonicum) strains on yield and growth of drought stressed soybean (Giza 111) plants at early pod stage (50 days from sowing, R3) and seed development stage (90 days from sowing, R5). RESULTS: Highest plant biomass, leaf chlorophyll content, nodulation, and grain yield were observed in the unstressed plants as compared with water stressed-plants at R3 and R5 stages. At soil rhizosphere level, AMF and B. japonicum treatments improved bacterial counts and the activities of the enzymes (dehydrogenase and phosphatase) under well-watered and drought stress conditions. Irrespective of the drought effects, AMF and B. japonicum treatments improved the growth and yield of soybean under both drought (restrained irrigation) and adequately-watered conditions as compared with untreated plants. The current study revealed that AMF and B. japonicum improved catalase (CAT) and peroxidase (POD) in the seeds, and a reverse trend was observed in case of malonaldehyde (MDA) and proline under drought stress. The relative expression of the CAT and POD genes was up-regulated by the application of biofertilizers treatments under drought stress condition. Interestingly a reverse trend was observed in the case of the relative expression of the genes involved in the proline metabolism such as P5CS, P5CR, PDH, and P5CDH under the same conditions. The present study suggests that biofertilizers diminished the inhibitory effect of drought stress on cell development and resulted in a shorter time for DNA accumulation and the cycle of cell division. There were notable changes in the activities of enzymes involved in the secondary metabolism and expression levels of GmSPS1, GmSuSy, and GmC-INV in the plants treated with biofertilizers and exposed to the drought stress at both R3 and R5 stages. These changes in the activities of secondary metabolism and their transcriptional levels caused by biofertilizers may contribute to increasing soybean tolerance to drought stress. CONCLUSIONS: The results of this study suggest that application of biofertilizers to soybean plants is a promising approach to alleviate drought stress effects on growth performance of soybean plants. The integrated application of biofertilizers may help to obtain improved resilience of the agro ecosystems to adverse impacts of climate change and help to improve soil fertility and plant growth under drought stress.

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Neupane J, Guo W. Agronomic basis and strategies for precision water management: a review. Agronomy. 2019;9(2):87. doi: 10.3390/agronomy9020087. DOI

Anonymous . Annual report international institute of tropical agriculture. Ibadan, Nigeria. 2000. pp. 1–2.

Soystats, American Soybean Association. http://soystats.com/ 2015 (accessed Mar 2017) (2015).

Buezo J, Sanz-Saez A, Jose MF, Soba D, Aranjuelo I, Esteban R. Drought tolerance response of high-yielding soybean varieties to mild drought: physiological and photochemical adjustments. Physiol Plant. 2019;166(1):88–104. doi: 10.1111/ppl.12864. PubMed DOI

Sheteiwy MS, Shao H, Qi W, Daly P, Sharma A, Shaghaleh H, Alhaj Hamoud Y, El-Esawi MA, Pan R, Wan Q, Lu H. Seed priming and foliar application with jasmonic acid enhance salinity stress tolerance of soybean (Glycine max, L.) seedlings. J Sci Food and Agric. 2020;2020:1–15. PubMed

Wakchaure G, Minhas P, Meena KK, Singh NP, Hegade PM, Sorty AM. Growth, bulb yield, water productivity and quality of onion (Allium cepa L.) as affected by deficit irrigation regimes and exogenous application of plant bio–regulators. Agric Water Manag. 2018;199:1–10. doi: 10.1016/j.agwat.2017.11.026. DOI

Li S, Xie Y, Liu G, Wang J, Lin H, Xin Y, Zhai J. Water use efficiency of soybean under water stress in different eroded soils. Water. 2020;12(2):373. doi: 10.3390/w12020373. DOI

Dai A. Drought under global warming: a review. Wires Clim Chg. 2012;2:45–65. doi: 10.1002/wcc.81. DOI

Manavalan LP, Guttikonda SK, Tran LP, Nguyen HT. Physiological and molecular approaches to improve drought resistance in soybean. Plant Cell Physiol. 2009;50(7):1260–1276. doi: 10.1093/pcp/pcp082. PubMed DOI

Purcell L. Specht J. physiological traits for ameliorating drought stress. In: Boerma H, Specht, editor. Soybeans: improvement, production, and uses. Madison WI: American Society of Agronomy; 2004. pp. 569–620.

Thao NP, Tran LS. Potentials toward genetic engineering of drought-tolerant soybean. Critical Rev Biotech. 2012;32(4):349–362. doi: 10.3109/07388551.2011.643463. PubMed DOI

Reddi GH, Reddi TY. Irrigation of principal crops, in: efficient use of irrigation water, 2nd ED; Kalyani Pub New Delhi. 1995. pp. 229–259.

Sheteiwy MS, Shao H, Qi W, Hamoud YA, Shaghaleh H, Khan NU, Yang R, Tang B. GABA-alleviated oxidative injury induced by salinity, osmotic stress and their combination by regulating cellular and molecular signals in rice. Int J Mol Sci. 2019;20(22):5709. doi: 10.3390/ijms20225709. PubMed DOI PMC

Wu R, Yang J, Wang L, Xiujuan G. Physiological response of flax seedlings with different drought-resistances to drought stress. Acta Agric Boreali-Sinica. 2019;34:145–153.

Hussain S, Pang T, Iqbal N, Shafiq I, Skalicky M, Brestic M, et al. Acclimation strategy and plasticity of different soybean genotypes in intercropping. Func Plant Biol. 2020:1–20. PubMed

Turkan I, Bor M, O¨zdemir F, Koca H Differential responses of lipid peroxidation and antioxidants in the leaves of drought-tolerant P acutifolius gray and drought-sensitive P vulgaris L subjected to polyethylene glycol mediated water stress Plant Sci 2005; 168: 223–231.

Sheteiwy MS, An J, Yin M, Jia X, Guan Y, He F, et al. Cold plasma treatment and exogenous salicylic acid priming enhances salinity tolerance of Oryza sativa seedlings. Protoplasma. 2018a:1–21. PubMed

Sheteiwy MS, Fu Y, Hu Q, Nawaz A, Guan Y, Zhan L, Huang Y, Hu J. Seed priming with polyethylene glycol induces antioxidative defense and metabolic performance of rice under nano-ZnO stress. Environ Sci Pollut Res. 2016;23(19):19989–20002. doi: 10.1007/s11356-016-7170-7. PubMed DOI

Sheteiwy MS, Shen H, Xu J, Guan Y, Song W, Hu J. Seed polyamines metabolism induced by seed priming with Spermidine and 5-aminolevulinic acid for chilling tolerance improvement in rice (Oryza sativa L.) seedlings. Environ Exp Bot. 2017;137:58–72. doi: 10.1016/j.envexpbot.2017.02.007. DOI

Sheteiwy MS, Dong Q, An J, Song W, Guan Y, He F, et al. Regulation of ZnO nanoparticles-induced physiological and molecular changes by seed priming with humic acid in Oryza sativa seedlings. Plant Growth Regul. 2017b:1–15.

Sheteiwy MS, Gong D, Gao Y, Pan R, Hu J, Guan Y. Priming with methyl jasmonate alleviates polyethylene glycol-induced osmotic stress in rice seeds by regulating the seed metabolic profile. Environ Exp Bot. 2018;153:236–248. doi: 10.1016/j.envexpbot.2018.06.001. DOI

Thu NBA, Nguyen QT, Hoang XLT, Thao NP, Tran LP. Evaluation of drought tolerance of the vietnamese soybean cultivars provides potential resources for soybean production and genetic engineering. Biomed Res Int. 2014;2014:1–10. doi: 10.1155/2014/809736. PubMed DOI PMC

Desclaux D, Huynh TT, Roumet P. Identification of soybean plant characteristics that indicate the timing of drought stress. Crop Sci. 2000;40(3):716–722. doi: 10.2135/cropsci2000.403716x. DOI

Kron AP, Souza GM, Ribeiro RV. Water deficiency at different developmental stages of Glycine max can improve drought tolerance. Bragantia. 2008;67(1):43–49. doi: 10.1590/S0006-87052008000100005. DOI

Lich MA, Wright D, Lenssen AW. Soybean response to drought, Agricultur. Iowa State University Extension and Outreach, Ames, IA (USA) (2013).

Hirasawa T, Tanaka K, Miyamoto D, Takei M, Ishihara K. Effects of pre-flowering moisture deficits on dry matter production and ecophysiological characteristics in soybean plants under drought conditions during grain filling. Jp J Crop Sci. 1994;63(4):721–730. doi: 10.1626/jcs.63.721. DOI

Andrade FH, Aguirrezábal LAN, Rizzalli RH, Crecimiento endimiento comparados. In: Andrade FH, Sadras VO (Eds.) Bases Para El Manejo Del Maíz, El Girasol Y La Soja. INTA Balcarce, Facultad de Ciencias Agrarias, Buenos Aires, Argentina p. 450 (2002).

Tarnabi ZM, Iranbakhsh A, Mehregan I, Ahmadvand R. Impact of arbuscular mycorrhizal fungi (AMF) on gene expression of some cell wall and membrane elements of wheat (Triticum aestivum L.) under water deficit using transcriptome analysis. Physiol Mol Biol Plants 2019; 1–20. PubMed PMC

Gao C, El-Sawah AM, Ali DFI, Alhaj Hamoud Y, Shaghaleh H, Sheteiwy MS. The Integration of bio and organic fertilizers improve plant growth, grain yield, quality and metabolism of hybrid maize (Zea mays L.) Agronomy. 2020;10:319. doi: 10.3390/agronomy10030319. DOI

Souza R, Ambrosini A, Passaglia LMP. Plant growth-promoting bacteria as inoculants in agricultural soils. Genet Mol Biol. 2015;38(4):401–419. doi: 10.1590/S1415-475738420150053. PubMed DOI PMC

Duc NH, Csintalan Z, Posta K. Arbuscular mycorrhizal fungi mitigate negative effects of combined drought and heat stress on tomato plants. Plant Physiol Bioch. 2018;132:297–307. doi: 10.1016/j.plaphy.2018.09.011. PubMed DOI

Baum C, El-Tohamy W, Gruda N. Increasing the productivity and product quality of vegetable crops using arbuscular mycorrhizal fungi: a review. Sci Hort. 2015;187:131–141. doi: 10.1016/j.scienta.2015.03.002. DOI

Rathod DP, Brestic M, Shao HB. Chlorophyll a fluorescence determines the drought resistance capabilities in two varieties of mycorhized and non-mycorrhized Glycine max Linn. Afric J Microbiol Res. 2011;5:4197–4206.

Augé RM. Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza. 2001;11:3–42. doi: 10.1007/s005720100097. DOI

Augé RM, Toler HD, Saxton AM. Arbuscular mycorrhizal symbiosis alters stomatal conductance of host plants more under drought than under amply watered conditions: a metal analysis. Mycorrhiza. 2015;25:13–24. doi: 10.1007/s00572-014-0585-4. PubMed DOI

Pedranzani H, Rodríguez-Rivera M, Gutiérrez M, Porcel R, Hause B, Ruiz-Lozano JM. Arbuscular mycorrhizal symbiosis regulates physiology and performance of Digitaria eriantha plants subjected to abiotic stresses by modulating antioxidant and jasmonate levels. Mycorrhiza. 2016;26(2):141–152. doi: 10.1007/s00572-015-0653-4. PubMed DOI

Quiroga G, Erice G, Aroca R, Chaumont F, Ruiz-Lozano JM. Enhanced drought stress tolerance by the arbuscular mycorrhizal symbiosis in drought-sensitive maize cultivar is related to a broader and differential regulation of host plant aquaporins than in a drought-tolerant cultivar. Front Plant Sci. 2017;8:1056. doi: 10.3389/fpls.2017.01056. PubMed DOI PMC

Chitarra W, Pagliarani C, Maserti B, Lumini E, Siciliano I, Cascone P, Schubert A, Gambino G, Balestrini R, Guerrieri E. Insights on the impact of arbuscular mycorrhizal symbiosis on tomato tolerance to water stress. Plant Physiol. 2016;171:1009–1023. doi: 10.1104/pp.16.00307. PubMed DOI PMC

Sawada H, Kuykendall LD, Young JM. Changing concepts in the systematics of bacterial nitrogen-fixing legume symbiosis. J Gen Appl Microbiol. 2003;49:155–179. doi: 10.2323/jgam.49.155. PubMed DOI

Stacey G, Libault M, Brechenmacher L, Wan J, May GD. Genetics and functional genomics of legume nodulation. Curr Opin Plant Biol. 2006;9:110–121. doi: 10.1016/j.pbi.2006.01.005. PubMed DOI

Hungria M, Vargas MAT. Environmental factors impacting N2 fixation in legumes grown in the tropics, with an emphasis on Brazil. Field Crop Res. 2000;65:151–164. doi: 10.1016/S0378-4290(99)00084-2. DOI

Tena W, Wolde-Meskel E, Walley F. Symbiotic efficiency of native and exotic rhizobium strains nodulating lentil (Lens culinaris Medik.) in soils of southern Ethiopia. Agronomy. 2016;6:1–11. doi: 10.3390/agronomy6010011. DOI

Htwe AZ, Moh SM, Moe K, Yamakawa T. Biofertiliser production for agronomic application and evaluation of its symbiotic effectiveness in soybeans. Agronomy. 2019;9(4):162. doi: 10.3390/agronomy9040162. DOI

Vincent JM. A manual for the practical study of the root- nodule bacteria. “IBP Handbook No. 15. Black well Sci., Pul. Oxford and Edinburgh. 1970; 54–58.

Ahmad F, Ahmad I, Khan MS. Indole acetic acid production by the indigenous isolates of Azotobacter and fluorescent Pseudomonas in the presence and absence of tryptophan. Turk J Bio. 2005;29:29–34.

Pikovskaya RI. Mobilization of phosphorus in soil in connection with vital activity of some microbial species. Mikrobiologiya. 1948;17:362–370.

Hemalatha N, Raja N, Jayachitra A, Rajalakshmi A, Valarmathi N. Isolation and characterization of phosphate solubilizing bacteria and analyzing their effect on Capsicum annum L. Int J Biol Pharm Res. 2013;4:159–167. doi: 10.7897/2230-8407.04735. DOI

Asrar A, Abdel-fattah GM, Elhindi KM. Improving growth, flower yield, and water relations of snapdragon (Antirhinum majus L.) plants grown under well-watered and water-stress conditions using arbuscular mycorrhizal fungi. Photosynthetica. 2012;50:305–316. doi: 10.1007/s11099-012-0024-8. DOI

Phillips JM, Hayman DS. Improved procedures for clearing roots and staining parasitic and vesicular arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Brit Mycol Soc. 1970;55(1):158–161. doi: 10.1016/S0007-1536(70)80110-3. DOI

Trouvelot A, Kough JL, Gianinazzi-Pearson V. Mesure du Taux de Mycorhization VA d’un Système Radiculaire Recherche de Methods D’estimation Ayant une Signification Fonctionnelle. In: Gianinazzi-Pearson V, Gianinazzi S, editors. Physiological and Genetical Aspects of Mycorrhizae. Paris: INRA Publications; 1986. pp. 217–221.

Gobran GR, Clegg S. A conceptual model for nutrient availability in the mineral soil-root system. Can J Soil Sci. 1996;76(2):125–131. doi: 10.4141/cjss96-019. DOI

Zhang X, Li F, Liu T, Xu C, Duan D, Peng C, et al. The variations in the soil enzyme activity, protein expression, microbial biomass, and community structure of soil contaminated by heavy metals. ISRN Soil Science. 2013:1–12.

Salah MS, Guan Y, Cao D, Li J, Nawaz A, Hu Q, Hu W, Ning M, Hu J. Seed priming with polyethylene glycol regulating the physiological and molecular mechanism in rice (Oryza sativa L.) under nano-ZnO stress. Sci Rep. 2015;5:14278. doi: 10.1038/srep14278. PubMed DOI PMC

Jiang JF, Lu YF, Li JG, Li L, He X, Shao HL, Dong YH. Effect of seed treatment by cold plasma on the resistance of tomato to Ralstonia solanacearum (bacterial wilt) PLoS One. 2014;9:1–6. PubMed PMC

Zhou WJ, Leul M. Uniconazole-induced tolerance of rape plants to heat stress in relation to changes in hormonal levels, enzyme activities and lipid peroxidation. Plant Growth Regul. 1999;27(2):99–104. doi: 10.1023/A:1006165603300. DOI

Hu Y, Zhang L, Zhao L, Li J, He S, Zhou K, Yang F, Huang M, Jiang L, Li L. Trichostatin a selectively suppresses the cold-induced transcription of the ZmDREB1 gene in maize. PLoS One. 2011;6(7):e22132. doi: 10.1371/journal.pone.0022132. PubMed DOI PMC

Igiehon NO, Babalola OO, Cheseto X, Torto B. Effects of rhizobia and arbuscular mycorrhizal fungi on yield, size distribution and fatty acid of soybean seeds grown under drought stress. Microbiol Res. 2021;242:126640. doi: 10.1016/j.micres.2020.126640. PubMed DOI

Iovieno P, Baath E. Effect of drying and rewetting on bacterial growth rates in soil. FEMS Microbiol Ecol. 2008;265:400–407. doi: 10.1111/j.1574-6941.2008.00524.x. PubMed DOI

Meisner A, Rousk J, Baath E. Prolonged drought changes the bacterial growth response to rewetting. Soil Biol Biochem. 2015;88:314–322. doi: 10.1016/j.soilbio.2015.06.002. DOI

Bloem J, De ruiter PC, Koopman GJ, Lebbink G, Brussaard L. Microbial numbers and activity in dried and rewetted arable soil under integrated and conventional management. Soil Biol Bioch. 1992;24:655–665. doi: 10.1016/0038-0717(92)90044-X. DOI

Juge C, Prévosta D, Bertranda A, Bipfubusaa M, Chalifourb FP. Growth and biochemical responses of soybean to double and triple microbial associations with Bradyrhizobium, Azospirillum and arbuscular mycorrhizae. Applied Soil Ecol. 2012;61:147–157. doi: 10.1016/j.apsoil.2012.05.006. DOI

Pavithra D, Yapa N. Arbuscular mycorrhizal fungi inoculation enhances drought stress tolerance of plants. Groundwater Sust Dev. 2018;7:490–494. doi: 10.1016/j.gsd.2018.03.005. DOI

Sinha RK, Valani D, Chauhan K, Agarwal S. Embarking on a second green revolution for sustainable agriculture by vermiculture biotechnology using earthworms: reviving the dreams of sir Charles Darwin. J Agric Technol Sustain Dev. 2010;2:113–128.

El-Sawah AM, El-Keblawy A, Ali DFI, Ibrahim HM, El-Sheikh MA, Sharma A, Alhaj Hamoud Y, Shaghaleh H, Brestic M, Skalicky M, Xiong YC, Sheteiwy MS. Arbuscular mycorrhizal fungi and plant growth-promoting rhizobacteria enhance soil key enzymes, plant growth, seed yield, and qualitative attributes of guar. Agriculture. 2021;11(3):194. doi: 10.3390/agriculture11030194. DOI

Jayne B, Quigley M. Influence of arbuscular mycorrhiza on growth and reproductive response of plants under water deficit: a meta-analysis. Mycorrhiza. 2014;24:109–119. doi: 10.1007/s00572-013-0515-x. PubMed DOI

Li T, Hu YJ, Hao ZP, Li H, Wang YS, Chen BD. First cloning and characterization of two functional aquaporin genes from an arbuscular mycorrhizal fungus Glomus intraradices. New Phytol. 2013;197:617–630. doi: 10.1111/nph.12011. PubMed DOI

Soe KM, Myint SS, Win MM, Aung TT, San KK, Myint SS. Co-inoculation of Myanmar Bradyrhizobium yuanmingense MAS34 and Streptomyces griseoflavus P4 inoculants to improve plant growth, seed yield of soybean cultivars and soil fertility improvement. Myanmar Agric Res J. 2018;4:154–164.

Hao Z, Xie W, Jiang X, Wu Z, Zhang X, Chen B. Arbuscular mycorrhizal fungus improves rhizobium–Glycyrrhiza seedling symbiosis under drought stress. Agronomy. 2019;9(10):572. doi: 10.3390/agronomy9100572. DOI

Buecking H, Kafle A. Role of Arbuscular Mycorrhizal fungi in the nitrogen uptake of plants: current knowledge and research gaps. Agronomy. 2015;5(4):587–612. doi: 10.3390/agronomy5040587. DOI

Goicoechea N, Merino S, Sanchez-Diaz M. Contribution of arbuscular mycorrhizal fungi (AMF) to the adaptations exhibited by the deciduous shrub Anthyllis cytisoides L. under water deficit. Physiol Plant. 2004;122(4):453–464. doi: 10.1111/j.1399-3054.2004.00421.x. DOI

Soe KM, Yamakawa T. Evaluation of effective Myanmar Bradyrhizobium strains isolated from Myanmar soybean and effects of co-inoculation with Streptomyces griseoflavus P4 for nitrogen fixation. Soil Sci Plant Nut. 2013;59(3):361–370. doi: 10.1080/00380768.2013.794437. DOI

Soe KM, Bhromsiri A, Karladee D, Yamakawa T. Effects of endophytic actinomycetes and Bradyrhizobium japonicum strains on growth, nodulation, nitrogen fixation and seed weight of different soybean varieties. Soil Sci Plant Nut. 2012;58(3):319–325. doi: 10.1080/00380768.2012.682044. DOI

Miao S, Shi H, Jin J, Liu J, Liu X, Wang G. Effects of short-term drought and flooding on soybean nodulation and yield at key nodulation stage under pot culture. J Food Agric Environ. 2012;10:819–824.

Mittler R. Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci. 2002;7(9):405–410. doi: 10.1016/S1360-1385(02)02312-9. PubMed DOI

Shah K, Kumar RG, Verma S, Dubey RS. Effect of cadmium on lipid peroxidation, superoxide anion generation and activities of antioxidant enzymes in growing rice seedlings. Plant Sci. 2001;161(6):1135–1144. doi: 10.1016/S0168-9452(01)00517-9. DOI

Lioussanne L, Perreault F, Jolicoeur M, St-Arnaud M. The bacterial community of tomato rhizosphere is modified by inoculation with arbuscular mycorrhizal fungi but unaffected by soil enrichment with mycorrhizal root exudates or inoculation with Phytophthora nicotianae. Soil Biol Biochem. 2010;42(3):473–483. doi: 10.1016/j.soilbio.2009.11.034. DOI

Kim SI, Tai TH. Evaluation of seedling cold tolerance in rice cultivars: a comparison of visual ratings and quantitative indicators of physiological changes. Euphytica. 2011;178(3):437–447. doi: 10.1007/s10681-010-0343-4. DOI

Choudhary NL, Sairam RK. Tyagi a, expression of Δ1-pyrroline-5-carboxylate synthetase gene during drought in rice (Oryza sativa L.) Indian J Biochem Biophys. 2005;42(6):366–370. PubMed

Dobra J, Vanková R, Havlová M, Burman AJ, Libus J, Štorchová H. Tobacco leaves and roots differ in the expression of proline metabolism-related genes in the course of drought stress and subsequent recovery. J Plant Physiol. 2011;168(13):1588–1597. doi: 10.1016/j.jplph.2011.02.009. PubMed DOI

Hien DT, Jacobs M, Angenon G, Hermans C, Thu TT, Son LV, Roosens NH. Proline accumulation and pyrroline-5-carboxylate synthetase gene properties in three rice cultivars differing in salinity and drought tolerance. Plant Sci. 2003;165(5):1059–1068. doi: 10.1016/S0168-9452(03)00301-7. DOI

Willett CS, Burton RS. Proline biosynthesis genes and their regulation under salinity stress in the euryhaline copepod Tigriopus californicus. Comp Biochem Physiol Part B. 2002;132(4):739–750. doi: 10.1016/S1096-4959(02)00091-X. PubMed DOI

Stein H, Honig A, Miller G, Erste O, Eilenberg H, Csonka LN, Szabados L, Koncz C, Zilberstein A. Elevation of free proline and proline-rich protein levels by simutaneous manipulations of proline biosynthesis and degradation in plants. Plant Sci. 2011;181(2):140–150. doi: 10.1016/j.plantsci.2011.04.013. PubMed DOI

Ma L, Zhou E, Gao L, Mao X, Zhou R, Jia J. Isolation, expression analysis and chromosomal location of P5CR gene in common wheat (Triticum aestivum L.). S. Afr J Bot. 2008;74(4):705–712. doi: 10.1016/j.sajb.2008.05.003. DOI

Szabados L, Savouré A. Proline: a multifunctional aminoacid. Trends Plant Sci. 2009;15:89–97. doi: 10.1016/j.tplants.2009.11.009. PubMed DOI

Zhao L, Wang P, Hou H, Zhang H, Wang Y, Yan S, Huang Y, Li H, Tan J, Hu A. Transcriptional regulation of cell cycle genes in response to abiotic stresses correlates with dynamic changes in histone modifications in maize. PLoS One. 2014;9(8):e106070. doi: 10.1371/journal.pone.0106070. PubMed DOI PMC

West G, Inze D, Beemster GT. Cell cycle modulation in the response of the primary root of Arabidopsis to salt stress. Plant Physiol. 2004;135(2):1050–1058. doi: 10.1104/pp.104.040022. PubMed DOI PMC

Santilli G, Schwab R, Watson R, Ebert C, Aronow BJ, Sala A. Temperature-dependent modification and activation of B-MYB: implications for cell survival. J Biol Chem. 2005;280(16):15628–15634. doi: 10.1074/jbc.M411747200. PubMed DOI

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