Abstract
Drought has been identified as a major factor restricting maize productivity worldwide, especially in the rainfed areas. The objective of the present study was to investigate the physiological adaptation strategies and sugar-related gene expression levels in three maize (Zea mays L.) genotypes with different drought tolerance abilities (Suwan4452, drought tolerant as a positive check; S7328, drought susceptible as a negative check; Pac339, drought susceptible) at the seedling stage. Ten-day old seedlings of maize genotypes were subjected to (i) well-watered (WW) or control and (ii) water-deficit (WD) conditions. Leaf osmotic potential of cv. S7328 under WD was significantly decreased by 1.35–1.45 folds compared with cv. Pac339 under WW, whereas it was retained in cv. Suwan4452, which utilized total soluble sugars as the major osmolytes for maintaining leaf greenness, Fv/Fm, ΦPSII, and stomatal function (Pn, net photosynthetic rate; gs, stomatal conductance; and E, transpiration rate). Interestingly, sucrose degradation (65% over the control) in cv. Pac339 under WD was evident in relation to the downregulation of the ZmSPS1 level, whereas glucose enrichment (1.65 folds over the control) was observed in relation to the upregulation of ZmSPS1 and ZmSUS1. Moreover, CWSI (crop water stress index), calculated from leaf temperature of stressed plants, was negatively correlated with E, gs, and Pn. Overall, growth characteristics, aboveground and belowground parts, in the drought-susceptible cv. Pac339 and cv. S7328, were significantly decreased (> 25% over the control), whereas these parameters in the drought-tolerant cv. Suwan4452 were unaffected. The study validates the use of leaf temperature, CWSI, Pn, gs, and E as sensitive parameters and overall growth characters as effective indices for drought tolerance screening in maize genotypes at the seedling stage. However, further experiments are required to validate the results observed in this study under field conditions.
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Abbreviations
- CWSI:
-
Crop water stress index
- Ci :
-
Intercellular CO2
- EC:
-
Electroconductivity
- Fv/Fm :
-
Maximum quantum yield of PSII
- Pn :
-
Net photosynthetic rate
- ΦPSII :
-
Photon yield of PSII
- SPP:
-
Sucrose-phosphate phosphatase
- SPS:
-
Sucrose-phosphate synthase
- gs :
-
Stomatal conductance
- SUS:
-
Sucrose synthase
- SWC:
-
Soil water content
- E:
-
Transpiration rate
- WD:
-
Water deficit
- WUE:
-
Water use efficiency
- WW:
-
Well-watered
References
Adamipour N, Khosh-Khui M, Salehi H, Razi H, Karami A, Moghadam A (2020) Metabolic and genes expression analyses involved in proline metabolism of two rose species under drought stress. Plant Physiol Biochem 155:105–113. https://doi.org/10.1016/j.plaphy.2020.07.028
Ahmad I, Ahmad B, Boote K, Hoogenboom G (2020) Adaptation strategies for maize production under climate change for semi-arid environments. Eur J Agron 115:126040. https://doi.org/10.1016/j.eja.2020.126040
Altuntaş C, Sezgin A, Demiralay M, Terzi R, Sağlam A, Kadioğlu A (2019) Application of sucrose modulates the expressions of genes involved in proline and polyamine metabolism in maize seedlings exposed to drought. Biol Plant 63:247–252. https://doi.org/10.32615/bp.2019.028
Anjum SA, Ashraf U, Tanveer M, Khan I, Hussain S, Shahzad B, Zohaib A, Abbas F, Saleem MF, Ali I, Wang LC (2017) Drought induced changes in growth, osmolyte accumulation and antioxidant metabolism of three maize hybrids. Front Plant Sci 8:69. https://doi.org/10.3389/fpls.2017.00069
Avramova V, AbdElgawad H, Zhang Z, Fotschki B, Casadevall R, Vergauwen L, Knapen D, Taleisnik E, Guisez Y, Asard H, Beemster GT (2015) Drought induces distinct growth response, protection, and recovery mechanisms in the maize leaf growth zone. Plant Physiol 169:1382–1396. https://doi.org/10.1104/pp.15.00276
Avramova V, Nagel KA, AbdElgawad H, Bustos D, DuPlessis M, Fiorani F, Beemster GTS (2016) Screening for drought tolerance of maize hybrids by multi-scale analysis of root and shoot traits at the seedling stage. J Exp Bot 67:2453–2466. https://doi.org/10.1093/jxb/erw055
Badr A, El-Shazly HH, Tarawneh RA, Börner A (2020) Screening for drought tolerance in maize (Zea mays L.) germplasm using germination and seedling traits under simulated drought conditions. Plants 9:565. https://doi.org/10.3390/plants9050565
Bandurska H, Niedziela J, Pietrowska-Borek M, Nuc K, Chadzinikolau T, Radzikowska D (2017) Regulation of proline biosynthesis and resistance to drought stress in two barley (Hordeum vulgare L.) genotypes of different origin. Plant Physiol Biochem 118:427–437. https://doi.org/10.1016/j.plaphy.2017.07.006
Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207. https://doi.org/10.1007/BF00018060
Baum ME, Licht MA, Huber I, Archontoulis SV (2020) Impacts of climate change on the optimum planting date of different maize cultivars in the central US Corn Belt. Eur J Agron 119:126101. https://doi.org/10.1016/j.eja.2020.126101
Cai F, Zhang Y, Mi N, Ming H, Zhang S, Zhang H, Zhao X (2020) Maize (Zea mays L.) physiological responses to drought and rewatering, and the associations with water stress degree. Agric Water Manag 241:106379. https://doi.org/10.1016/j.agwat.2020.106379
Carroll DA, Hansen NC, Hopkins BG, DeJonge KC (2017) Leaf temperature of maize and Crop Water Stress Index with variable irrigation and nitrogen supply. Irrig Sci 35:549–560. https://doi.org/10.1007/s00271-017-0558-4
Cha-um S, Supaibulwatana K, Kirdmanee C (2006) Water relation, photosynthetic ability and growth of Thai jasmine rice (Oryza sativa L. ssp. indica cv. KDML 105) to salt stress by application of exogenous glycinebetaine and choline. J Agron Crop Sci 192:25–36. https://doi.org/10.1111/j.1439-037X.2006.00186.x
Chen D, Wang S, Cao B, Cao D, Leng G, Li H, Yin L, Shan L, Deng X (2016a) Genotypic variation in growth and physiological response to drought stress and re-watering reveals the critical role of recovery in drought adaptation in maize seedlings. Front Plant Sci 6:1241. https://doi.org/10.3389/fpls.2015.01241
Chen T, Xia G, Liu T, Chen W, Chi D (2016b) Assessment of drought impact on main cereal crops using a standardized precipitation evapotranspiration index in Liaoning Province. China Sustainability 8:1069. https://doi.org/10.3390/su8101069
Choudhary NL, Sairam RK, Tyagi A (2005) Expression of Δ1-pyrroline-5-carboxylate synthetase gene during drought in rice (Oryza sativa L.). Indian J Biochem Biophys 42:366–370
Costa JM, Grant OM, Chaves MM (2013) Thermography to explore plant-environment interactions. J Exp Bot 64:3937–3949. https://doi.org/10.1093/jxb/ert029
Cuellar-Ortiz SM, Arrieta-Montiel MDLP, Acosta-Gallegos J, Covarrubias AA (2008) Relationship between carbohydrate partitioning and drought resistance in common bean. Plant Cell Environ 31:1399–1409. https://doi.org/10.1111/j.1365-3040.2008.01853.x
Dalezios NR, Angelakis AN, Eslamian S (2018) Water scarcity management: Part 1: Methodological framework. Int J Glob Environ Issue 17:1–40. https://doi.org/10.1504/IJGENVI.2018.090629
DeJonge KC, Taghvaeian S, Trout TJ, Comas LH (2015) Comparison of canopy temperature-based water stress indices for maize. Agric Water Manag 156:51–62. https://doi.org/10.1016/j.agwat.2015.03.023
Elliott J, Glotter M, Ruane AC, Boote KJ, Hatfield JL, Jones JW, Rosenzweig C, Smith LA, Foster I (2018) Characterizing agricultural impacts of recent large-scale US droughts and changing technology and management. Agric Syst 159:275–281. https://doi.org/10.1016/j.agsy.2017.07.012
Fu J, Huang B, Fry J (2010) Osmotic potential, sucrose level, and activity of sucrose metabolic enzymes in tall fescue in response to deficit irrigation. J Am Soc Hortic Sci 135:506–510. https://doi.org/10.21273/JASHS.135.6.506
Hayano-Kanashiro C, Calderón-Vázquez C, Ibarra-Laclette E, Herrera-Estrella L, Simpson J (2009) Analysis of gene expression and physiological responses in three Mexican maize landraces under drought stress and recovery irrigation. PLoS ONE 4:e7531. https://doi.org/10.1371/journal.pone.0007531
He X, Estes L, Konar M, Tian D, Anghileri D, Baylis K, Evans TP, Sheffield J (2019) Integrated approaches to understanding and reducing drought impact on food security across scales. Curr Opin Environ Sust 40:43–54. https://doi.org/10.1016/j.cosust.2019.09.006
Hussain F, Bronson KF, Peng S (2000) Use of chlorophyll meter sufficiency indices for nitrogen management of irrigated rice in Asia. Agron J 92:875–879. https://doi.org/10.2134/agronj2000.925875x
Jones HG, Schofield P (2008) Thermal and other remote sensing of plant stress. Gen Appl Plant Physiol 34:19–32
Jones HG, Serraj R, Loveys BR, Xiong L, Wheaton A, Price AH (2009) Thermal infrared imaging of crop canopies for the remote diagnosis and quantification of plant responses to water stress in the field. Funct Plant Biol 36:978–989. https://doi.org/10.1071/FP09123
Kakani VG, Vu JC Jr, Allen LH, Boote KJ (2011) Leaf photosynthesis and carbohydrates of CO2-enriched maize and grain sorghum exposed to a short period of soil water deficit during vegetative development. J Plant Physiol 168:2169–2176. https://doi.org/10.1016/j.jplph.2011.07.003
Kakumanu A, Ambavaram MM, Klumas C, Krishnan A, Batlang U, Myers E, Grene R, Pereira A (2012) Effects of drought on gene expression in maize reproductive and leaf meristem tissue revealed by RNA-Seq. Plant Physiol 160:846–867. https://doi.org/10.1104/pp.112.200444
Karkacier M, Erbas M, Uslu MK, Aksu M (2003) Comparison of different extraction and detection methods for sugars using amino-bonded phase HPLC. J Chromatog Sci 41:331–333. https://doi.org/10.1093/chromsci/41.6.331
Kucharik CJ (2008) Contribution of planting date trends to increased maize yields in the central United States. Agron J 100:328–336. https://doi.org/10.2134/agronj2007.0145
Kumari M, Dass S, Vimala Y, Arora P (2004) Physiological parameters governing drought tolerance in maize. Indian J Plant Physiol 9:203–207
Legay S, Lefèvre I, Lamoureux D, Barreda C, Luz RT, Gutierrez R, Quiroz R, Hoffmann L, Hausman JF, Bonierbale M, Ever D, Schafleitner R (2011) Carbohydrate metabolism and cell protection mechanisms differentiate drought tolerance and sensitivity in advanced potato clones (Solanum tuberosum L.). Funct Integr Genom 11:275–291. https://doi.org/10.1007/s10142-010-0206-z
Leng G, Hall J (2019) Crop yield sensitivity of global major agricultural countries to droughts and the projected changes in the future. Sci Total Environ 654:811–821. https://doi.org/10.1016/j.scitotenv.2018.10.434
Li Y, Sun C, Huang Z, Pan J, Wang L, Fan X (2009) Mechanisms of progressive water deficit tolerance and growth recovery of Chinese maize foundation genotypes Huangzao 4 and Chang 7–2, which are proposed on the basis of comparison of physiological and transcriptomic responses. Plant Cell Physiol 50:2092–2111. https://doi.org/10.1093/pcp/pcp145
Li Y, Song H, Zhou L, Xu Z, Zhou G (2019a) Tracking chlorophyll fluorescence as an indicator of drought and rewatering across the entire leaf lifespan in a maize field. Agric Water Manag 211:190–201. https://doi.org/10.1016/j.agwat.2018.09.050
Li CF, Dong ST, Liu RX, Ren H, Ding ZS, Zhao M (2019b) Diurnal variation of gas exchange, chlorophyll fluorescence, and photosynthetic response of six parental lines of maize released in three eras. J Integr Agric 18:2732–2741. https://doi.org/10.1016/S2095-3119(19)62693-6
Lima RSN, García-Tejero I, Lopes TS, Costa JM, Vaz M, Durán-Zuazo VH, Chaves M, Glenn DM, Campostrini E (2016) Linking thermal imaging to physiological indicators in Carica papaya L. under different watering regimes. Agric Water Manag 164:148–157. https://doi.org/10.1016/j.agwat.2015.07.017
Lin Y, Zhang C, Lan H, Gao S, Liu H, Liu J, Pan G, Rong T, Zhang S (2014) Validation of potential reference genes for qPCR in maize across abiotic stresses, hormone treatments, and tissue types. PLoS ONE 9:e95445. https://doi.org/10.1371/journal.pone.0095445
Liu Y, Subhash C, Yan J, Song C, Zhao J, Li J (2011) Maize leaf temperature responses to drought: thermal imaging and quantitative trait loci (QTL) mapping. Environ Exp Bot 71:158–165. https://doi.org/10.1016/j.envexpbot.2010.11.010
Liu Y, Wang L, Li Y, Li X, Zhang J (2019) Proline metabolism-related gene expression in four potato genotypes in response to drought stress. Biol Plant 63:757–764. https://doi.org/10.32615/bp.2019.153
Liu S, Wu W, Yang X, Yang P, Sun J (2020) Exploring drought dynamics and its impacts on maize yield in the Huang-Huai-Hai farming region of China. Clim Chang 163:415–430. https://doi.org/10.1007/s10584-020-02880-6
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. https://doi.org/10.1006/meth.2001.1262
Loggini B, Scartazza A, Brugnoli E, Navari-Izzo F (1999) Antioxidant defense system, pigment composition, and photosynthetic efficiency in two wheat cultivars subjected to drought. Plant Physiol 119:1091–1099. https://doi.org/10.1104/pp.119.3.1091
Lu Y, Hao Z, Xie C, Crossa J, Araus JL, Gao S, Vivek BS, Magorokosho C, Mugo S, Makumbi D, Taba S, Pan G, Li X, Rong T, Zhang S, Xu Y (2011) Large-scale screening for maize drought resistance using multiple selection criteria evaluated under water-stressed and well-watered environments. Field Crops Res 124:37–45. https://doi.org/10.1016/j.fcr.2011.06.003
Lunduka RW, Mateva KI, Magorokosho C, Manjeru P (2019) Impact of adoption of drought-tolerant maize varieties on total maize production in south Eastern Zimbabwe. Clim Dev 11:35–46. https://doi.org/10.1080/17565529.2017.1372269
Ma X, He Q, Zhou G (2018) Sequence of changes in maize responding to soil water deficit and related critical thresholds. Front Plant Sci 9:511. https://doi.org/10.3389/fpls.2018.00511
Maghsoudi K, Emam Y, Niazi A, Pessarakli M, Arvin MJ (2018) P5CS expression level and proline accumulation in the sensitive and tolerant wheat cultivars under control and drought stress conditions in the presence/absence of silicon and salicylic acid. J Plant Interact 13:461–471. https://doi.org/10.1080/17429145.2018.1506516
Manning DT, Lurbé S, Comas LH, Trout TJ, Flynn N, Fonte SJ (2018) Economic viability of deficit irrigation in the Western US. Agric Water Manag 196:114–123. https://doi.org/10.1016/j.agwat.2017.10.024
Manoli A, Sturaro A, Trevisan S, Quaggiotti S, Nonis A (2012) Evaluation of candidate reference genes for qPCR in maize. J Plant Physiol 169:807–815. https://doi.org/10.1016/j.jplph.2012.01.019
Maxwell K, Johnson GN (2000) Chlorophyll fluorescence – a practical guide. J Exp Bot 51:659–668. https://doi.org/10.1093/jexbot/51.345.659
McLaughlin JE, Boyer JS (2004) Sugar-responsive gene expression, invertase activity, and senescence in aborting maize ovaries at low water potentials. Ann Bot 94:675–689. https://doi.org/10.1093/aob/mch193
Meron M, Tsipris J, Orlov V, Alchanatis V, Cohen Y (2010) Crop water stress mapping for site-specific irrigation by thermal imagery and artificial reference surfaces. Precis Agric 11:148–162. https://doi.org/10.1007/s11119-009-9153-x
Moradi R, Koocheki A, Mahallati MN, Mansoori H (2013) Adaptation strategies for maize cultivation under climate change in Iran: irrigation and planting date management. Mitig Adap Strat Glob Chang 18:265–284. https://doi.org/10.1007/s11027-012-9410-6
Murray-Tortarolo GN, Jaramillo VJ, Larsen J (2018) Food security and climate change: the case of rainfed maize production in Mexico. Agric Forest Meteorol 253:124–131. https://doi.org/10.1016/j.agrformet.2018.02.011
Nikolaeva MK, Maevskaya SN, Voronin PY (2015) Activities of antioxidant and osmoprotective systems and photosynthetic gas exchange in maize seedlings under drought conditions. Russian J Plant Physiol 62:314–321. https://doi.org/10.1134/S1021443715030139
O’Shaughnessy SA, Andrade MA, Evett SR (2017) Using an integrated crop water stress index for irrigation scheduling of two corn hybrids in a semi-arid region. Irrig Sci 35:451–467. https://doi.org/10.1007/s00271-017-0552-x
Parida AK, Dagaonkar VS, Phalak MS, Aurangabadkar LP (2008) Differential responses of the enzymes involved in proline biosynthesis and degradation in drought tolerant and sensitive cotton genotypes during drought stress and recovery. Acta Physiol Plant 30:619–627. https://doi.org/10.1007/s11738-008-0157-3
Pelleschi S, Rocher JP, Prioul JL (1997) Effect of water restriction on carbohydrate metabolism and photosynthesis in mature maize leaves. Plant Cell Environ 20:493–503. https://doi.org/10.1046/j.1365-3040.1997.d01-89.x
Ramirez-Cabral NY, Kumar L, Shabani F (2017) Global alterations in areas of suitability for maize production from climate change and using a mechanistic species distribution model (CLIMEX). Sci Rep 7:5910. https://doi.org/10.1038/s41598-017-05804-0
Ranum P, Peña-Rosas JP, Garcia-Casal MN (2014) Global maize production, utilization, and consumption. Ann New York Acad Sci 1312:105–112. https://doi.org/10.1111/nyas.12396
Raynolds SG (1970) The gravimetric method of soil moisture determination. Part I. A study of equipment, and methodological problems. J Hydrol 11:258–273. https://doi.org/10.1016/0022-1694(70)90066-1
Romano G, Zia S, Spreer W, Sanchez C, Cairns J, Araus JL, Müller J (2011) Use of thermography for high throughput phenotyping of tropical maize adaptation in water stress. Comput Electron Agric 79:67–74. https://doi.org/10.1016/j.compag.2011.08.011
Ruan YL (2014) Sucrose metabolism: gateway to diverse carbon use and sugar signaling. Ann Rev Plant Biol 65:33–67. https://doi.org/10.1146/annurev-arplant-050213-040251
Schafleitner R, Gaudin A, Rosales ROG, Aliaga CAA, Bonierbale M (2007) Proline accumulation and real time PCR expression analysis of genes encoding enzymes of proline metabolism in relation to drought tolerance in Andean potato. Acta Physiol Plant 29:19–26. https://doi.org/10.1007/s11738-006-0003-4
Song H, LiY ZL, Xu Z, Zhou G (2018) Maize leaf functional responses to drought episode and rewatering. Agric Forest Meteorol 249:57–70. https://doi.org/10.1016/j.agrformet.2017.11.023
Song X, Zhou G, He Q, Zhou H (2020) Stomatal limitations to photosynthesis and their critical water conditions in different growth stages of maize under water stress. Agric Water Manag 241:106330. https://doi.org/10.1016/j.agwat.2020.106330
Tietjen B, Schlaepfer DR, Bradford JB, Lauenroth WK, Hall SA, Duniway MC, Hochst T, Jia G, Munson SM, Pyke DA, Wilson SD (2017) Climate change-induced vegetation shifts lead to more ecological droughts despite projected rainfall increases in many global temperate drylands. Glob Chang Biol 23:2743–2754. https://doi.org/10.1111/gcb.13598
Voronin PY, Maevskaya SN, Nikolaeva MK (2019) Physiological and molecular responses of maize (Zea mays L.) plants to drought and rehydration. Photosynthetica 57:850–856. https://doi.org/10.32615/ps.2019.101
Wei T, Wang Y, Xie Z, Guo D, Chen C, Fan Q, Deng X, Liu JH (2019) Enhanced ROS scavenging and sugar accumulation contribute to drought tolerance of naturally occurring autotetraploids in Poncirus trifoliata. Plant Biotechnol J 17:1394–1407. https://doi.org/10.1111/pbi.13064
West H, Quinn N, Horswell M (2019) Remote sensing for drought monitoring & impact assessment: progress, past challenges, and future opportunities. Remote Sens Environ 232:111291. https://doi.org/10.1016/j.rse.2019.111291
Wiriya-Alongkorn W, Spreer W, Ongprasert S, Spohrer K, Pankasemsuk T, Muller J (2013) Detecting drought stress in longan tree using thermal imaging. Maejo Int J Sci Technol 7:166–180
Wossen T, Abdoulaye T, Alene A, Feleke S, Menkir A, Manyong V (2017) Measuring the impacts of adaptation strategies to drought stress: the case of drought tolerant maize varieties. J Environ Manag 203:106–113. https://doi.org/10.1016/j.jenvman.2017.06.058
Xue GP, McIntyre CL, Glassop D, Shorter R (2008) Use of expression analysis to dissect alterations in carbohydrate metabolism in wheat leaves during drought stress. Plant Mol Biol 67:197–214. https://doi.org/10.1007/s11103-008-9311-y
Yu LX, Setter TL (2003) Comparative transcriptional profiling of placenta and endosperm in developing maize kernels in response to water deficit. Plant Physiol 131:568–582. https://doi.org/10.1104/pp.014365
Žalud Z, Hlavinka P, Prokeš K, Semerádová D, Jan B, Trnka M (2017) Impacts of water availability and drought on maize yield – a comparison of 16 indicators. Agric Water Manag 188:126–135. https://doi.org/10.1016/j.agwat.2017.04.007
Zampieri M, Ceglar A, Dentener F, Dosio A, Naumann G, van Den Berg M, Toreti A (2019) When will current climate extremes affecting maize production become the norm? Earth’s Future 7:113–122. https://doi.org/10.1029/2018EF000995
Zhang Q, Liu H, Wu X, Wang W (2020) Identification of drought tolerant mechanisms in a drought-tolerant maize mutant based on physiological, biochemical and transcriptomic analyses. BMC Plant Biol 20:315. https://doi.org/10.1186/s12870-020-02526-w
Zhang X, Lei L, Lai J, Zhao H, Song W (2018) Effects of drought stress and water recovery on physiological responses and gene expression in maize seedlings. BMC Plant Biol 18:68. https://doi.org/10.1186/s12870-018-1281-x
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The authors sincerely thank the Agricultural Research Development Agency (ARDA Grant Number: PRP5905020180) and the National Science and Technology Development Agency (NSTDA), Thailand, for financial support of this work.
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This work was sponsored by the Agricultural Research Development Agency (ARDA; grant number PRP5905020180).
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Suriyan Cha-um: Project leader, experimental layout, manuscript preparation, and edited version. Piyanan Pipatsitee: Plant material preparation, data collection, and analysis. Rujira Tiasarum and Cattarin Theerawitaya: mRNA expression level and physiological data collection and analysis. Thapanee Samphumphuang: Free proline and total soluble sugar analysis using HPLC and data analysis, measuring of morphological, and overall growth characteristics. Harminder Pal Singh and Avishek Datta: manuscript editing, data analysis, and English language proofing.
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Pipatsitee, P., Theerawitaya, C., Tiasarum, R. et al. Physio-morphological traits and osmoregulation strategies of hybrid maize (Zea mays) at the seedling stage in response to water-deficit stress. Protoplasma 259, 869–883 (2022). https://doi.org/10.1007/s00709-021-01707-0
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DOI: https://doi.org/10.1007/s00709-021-01707-0