Abstract
Main conclusion
Morpho-physiological changes were observed in Arabidopsis plants acclimated to long-term combined cold and water deficit stresses. Limiting growth and differences in bolting, flowering, and silique development were evidenced.
Abstract
In nature, plants are exposed to multiple and simultaneous abiotic stresses that influence their growth, development, and reproduction. In the last years, the study of combined stresses has aroused the interest to know the physiological and molecular responses, because these new stress conditions are probed to be different from the sum of the individual stress. We are interested in the study of the acclimation of plants growing under the combination of cold and water deficit stresses prevalent in cold-arid or semi-arid climates worldwide. We hypothesized that the reproduction of the acclimated plants will be compromised and affected. Arabidopsis plants were submitted to long-term combined stress from the beginning to the reproductive stage, when floral bud was visible, until the silique development. Our results demonstrate severe morpho-anatomical changes after acclimation to combined stress. Inflorescence stem morphology was altered having a delayed bolting and a limited growth. Flowering and silique formation were delayed, and a higher size in the corolla and the petals was observed. Flower and silique number were severely diminished as a result of combined stress, unlike acclimated plants to individual cold stress. These traits were recovered after deacclimation to optimal conditions and plants achieved similar silique production as control plants. The long-term stress results suggest that there is not a single dominant stress, but there is an alternating dominance depending on the structure or the plant stage development evaluated.
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Abbreviations
- C + WD:
-
Cold and water deficit
- RWC:
-
Relative water content
- ROS:
-
Reactive oxygen species
- WD:
-
Water deficit
References
Atkin OK, Loveys BR, Atkinson LJ, Pons TL (2006) Phenotypic plasticity and growth temperature: understanding interspecific variability. J Exp Bot 57(2):267–281. https://doi.org/10.1093/jxb/erj029
Bartels D, Sunkar R (2005) Drought and salt tolerance in plants. CRC Crit Rev Plant Sci 24:23–58. https://doi.org/10.1080/07352680590910410
Battaglia M, Olvera-Carrillo Y, Garciarrubio A, Campos F, Covarrubias AA (2008) The enigmatic LEA proteins and other hydrophilins. Plant Physiol 148(1):6–24. https://doi.org/10.1104/pp.108.120725
Berry JC, Fahlgren N, Pokorny AA, Bart RS, Veley KM (2018) An automated, high-throughput method for standardizing image color profiles to improve image-based plant phenotyping. PeerJ 6:e5727. https://doi.org/10.7717/peerj.5727
Boyes DC, Zayed AM, Ascenzi R, McCaskill AJ, Hoffman NE, Davis KR, Görlach J (2001) Growth stage–based phenotypic analysis of Arabidopsis: a model for high throughput functional genomics in plants. Plant Cell 13(7):1499–1510. https://doi.org/10.1105/TPC.010011
Castelan-Muñoz N, Herrera J, Cajero-Sanchez W, Arrizubieta M, Trejo C, Garcia-Ponce B, Sanchez MP, Alvarez-Buylla ER, Garay-Arroyo A (2019) MADS-Box genes are key components of genetic regulatory networks involved in abiotic stress and plastic developmental Responses in plants. Front Plant Sci 10:853. https://doi.org/10.3389/fpls.2019.00853
Chen C, Huang W, Hou K, Wu W (2019) Bolting, an important process in plant development, two types in plants. J Plant Biol 62(3):161–169. https://doi.org/10.1007/s12374-018-0408-9
Demirel U, Morris WL, Ducreux LJM, Yavuz C, Asim A, Tindas I, Campbell R, Morris JA, Verrall SR, Hedley PE, Gokce ZNO, Caliskan S, Aksoy E, Caliskan ME, Taylor MA, Hancock RD (2020) Physiological, biochemical, and transcriptional responses to single and combined abiotic stress in stress-tolerant and stress-sensitive potato genotypes. Front Plant Sci 11:169. https://doi.org/10.3389/fpls.2020.00169
Ding Y, Shi Y, Yang S (2019) Advances and challenges in uncovering cold tolerance regulatory mechanisms in plants. New Phytol 222(4):1690–1704. https://doi.org/10.1111/nph.15696
Dinneny JR (2019) Developmental responses to water and salinity in root systems. Annu Rev Cell Dev Biol 35(1):239–257. https://doi.org/10.1146/annurev-cellbio-100617-062949
Fang X, Turner NC, Yan G, Li F, Siddique KHM (2009) Flower numbers, pod production, pollen viability, and pistil function are reduced and flower and pod abortion increased in chickpea (Cicer arietinum L.) under terminal drought. J Exp Bot 61(2):335–345. https://doi.org/10.1093/jxb/erp307
Fernández OA, Busso CA (1999) Arid and semi-arid rangelands: two thirds of Argentina. Rala Report No. 200. Agricultural Research Institute, Keldnaholt, 112 Reykjavik, Iceland
Fowler S, Thomashow MF (2002) Arabidopsis transcriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition to the CBF cold response pathway. Plant Cell 14(8):1675–1690. https://doi.org/10.1105/tpc.003483
Fürtauer L, Weiszmann J, Weckwerth W, Nägele T (2019) Dynamics of plant metabolism during cold acclimation. Int J Mol Sci 20(21):5411. https://doi.org/10.3390/ijms20215411
Gehan MA, Fahlgren N, Abbasi A, Berry JC, Callen ST, Chavez L, Doust AN, Feldman MJ, Gilbert KB, Hodge JG, Hoyer JS, Lin A, Liu S, Lizárraga C, Lorence A, Miller M, Platon E, Tessman M, Sax T (2017) PlantCV v2: image analysis software for high-throughput plant phenotyping. PeerJ 5:e4088. https://doi.org/10.7717/peerj.4088
Guo Q, Liu L, Barkla BJ (2019) Membrane lipid remodeling in response to salinity. Int J Mol Sci 20(17):4264. https://doi.org/10.3390/ijms20174264
Hannah MA, Heyer AG, Hincha DK (2005) A global survey of gene regulation during cold acclimation in Arabidopsis thaliana. PLoS Genet 1(2):e26
Harb A, Krishnan A, Ambavaram MMR, Pereira A (2010) Molecular and physiological analysis of drought stress in Arabidopsis reveals early responses leading to acclimation in plant growth. Plant Physiol 154(3):1254–1271. https://doi.org/10.1104/pp.110.161752
Hepworth J, Dean C (2015) Flowering Locus C’s lessons: conserved chromatin switches underpinning developmental timing and adaptation. Plant Physiol 168(4):1237–1245. https://doi.org/10.1104/pp.15.00496
Hussain HA, Men S, Hussain S, Zhang Q, Ashraf U, Anjum SA, Ali I, Wang L (2020) Maize tolerance against drought and chilling stresses varied with root morphology and antioxidative defense system. Plants 9(6):720. https://doi.org/10.3390/plants9060720
Iyer NJ, Tang Y, Mahalingam R (2013) Physiological, biochemical and molecular responses to a combination of drought and ozone in Medicago truncatula. Plant Cell Environ 36(3):706–720. https://doi.org/10.1111/pce.12008
Janská A, Maršík P, Zelenková S, Ovesná J (2010) Cold stress and acclimation—what is important for metabolic adjustment? Plant Biol 12(3):395–405. https://doi.org/10.1111/j.1438-8677.2009.00299.x
Johnson I, Alexander S (2017) The global land outlook. Convention to combat desertification, United Nations, Bonn, Germany
Kaplan F, Kopka J, Sung DY, Zhao W, Popp M, Porat R, Guy CL (2007) Transcript and metabolite profiling during cold acclimation of Arabidopsis reveals an intricate relationship of cold-regulated gene expression with modifications in metabolite content. Plant J 50(6):967–981. https://doi.org/10.1111/j.1365-313X.2007.03100.x
Kiran A, Kumar S, Nayyar H, Sharma KD (2019) Low temperature-induced aberrations in male and female reproductive organ development cause flower abortion in chickpea. Plant Cell Environ 42(7):2075–2089. https://doi.org/10.1111/pce.13536
Koevoets IT, Venema JH, Elzenga JTM, Testerink C (2016) Roots withstanding their environment: exploiting root system architecture responses to abiotic stress to improve crop tolerance. Front Plant Sci 7:1335. https://doi.org/10.3389/fpls.2016.01335
Kollist H, Zandalinas SI, Sengupta S, Nuhkat M, Kangasjärvi J, Mittler R (2019) Rapid responses to abiotic stress: priming the landscape for the signal transduction network. Trends Plant Sci 24(1):25–37. https://doi.org/10.1016/j.tplants.2018.10.003
Kovinich N, Kayanja G, Chanoca A, Riedl K, Otegui MS, Grotewold E (2014) Not all anthocyanins are born equal: distinct patterns induced by stress in Arabidopsis. Planta 240(5):931–940. https://doi.org/10.1007/s00425-014-2079-1
Kuromori T, Seo M, Shinozaki K (2018) ABA transport and plant water stress responses. Trends Plant Sci 23(6):513–522. https://doi.org/10.1016/j.tplants.2018.04.001
Laban P, Metternicht G, Davies J (2018) Soil biodiversity and soil organic carbon: keeping drylands alive. Int Union for Conservation of Nature (IUCN), Gland. https://doi.org/10.2305/IUCN.CH.2018.03.en
Lantzouni O, Alkofer A, Falter-Braun P, Schwechheimer C (2020) GROWTH-REGULATING FACTORS interact with DELLAs and regulate growth in cold stress. Plant Cell 32(4):1018–1034. https://doi.org/10.1105/tpc.19.00784
Liu W, Zhou Y, Li X, Wang X, Dong Y, Wang N, Liu X, Chen H, Yao N, Cui X, Jameel A, Wang F, Li H (2017) Tissue-specific regulation of Gma-miR396 family on coordinating development and low water availability responses. Front Plant Sci 8:1112. https://doi.org/10.3389/fpls.2017.01112
Locquin M, Langeron M (1983) Staining and impregnation. Handbook of microscopy, 1st edn. Butterworth & Co, Paddington, pp 194–209
Loka DA, Oosterhuis DM, Baxevanos D, Noulas C, Hu W (2020) Single and combined effects of heat and water stress and recovery on cotton (Gossypium hirsutum L.) leaf physiology and sucrose metabolism. Plant Physiol Biochem 148:166–179. https://doi.org/10.1016/j.plaphy.2020.01.015
Ma X, Sukiran N, Ma H, Su Z (2014) Moderate drought causes dramatic floral transcriptomic reprogramming to ensure successful reproductive development in Arabidopsis. BMC Plant Biol 14(1):164. https://doi.org/10.1186/1471-2229-14-164
Mahalingam R (2015) Consideration of combined stress: a crucial paradigm for improving multiple stress tolerance in plants. In: Mahalingam R (ed) Combined stresses in plants. Springer, Cham, pp 1–25. https://doi.org/10.1007/978-3-319-07899-1_1
Mita S, Murano N, Akaike M, Nakamura K (1997) Mutants of Arabidopsis thaliana with pleiotropic effects on the expression of the gene for beta-amylase and on the accumulation of anthocyanin that are inducible by sugars. Plant J 11(4):841–851. https://doi.org/10.1046/j.1365-313X.1997.11040841.x
Mittler R (2006) Abiotic stress, the field environment and stress combination. Trends Plant Sci 11(1):15–19. https://doi.org/10.1016/j.tplants.2005.11.002
Munné-Bosch S, Queval G, Foyer CH (2013) The impact of global change factors on redox signaling underpinning stress tolerance. Plant Physiol 161(1):5–19. https://doi.org/10.1104/pp.112.205690
O’Brien T, Feder N, McCully M (1964) Polychromatic staining of plant cell walls by toluidine blue O. Protoplasma 59:368–373. https://doi.org/10.1007/BF01248568
Pandey P, Ramegowda V, Senthil-Kumar M (2015) Shared and unique responses of plants to multiple individual stresses and stress combinations: physiological and molecular mechanisms. Front Plant Sci 6:723–737. https://doi.org/10.3389/fpls.2015.00723
Pastori GM, Foyer CH (2002) Common components, networks, and pathways of cross-tolerance to stress. The central role of “redox” and abscisic acid-mediated controls. Plant Physiol 129(2):460–468. https://doi.org/10.1104/pp.011021
Rabino I, Mancinelli AL (1986) Light, temperature, and anthocyanin production. Plant Physiol 81(3):922–924. https://doi.org/10.1104/pp.81.3.922
Rasmussen S, Barah P, Suarez-Rodriguez MC, Bressendorff S, Friis P, Costantino P, Bones AM, Nielsen HB, Mundy J (2013) Transcriptome responses to combinations of stresses in Arabidopsis. Plant Physiol 161(4):1783–1794. https://doi.org/10.1104/pp.112.210773
Rivero RM, Mestre TC, Mittler RON, Rubio F, Garcia-Sanchez F, Martinez V (2014) The combined effect of salinity and heat reveals a specific physiological, biochemical and molecular response in tomato plants. Plant Cell Environ 37(5):1059–1073. https://doi.org/10.1111/pce.12199
Rizhsky L (2002) The combined effect of drought stress and heat shock on gene expression in tobacco. Plant Physiol 130(3):1143–1151. https://doi.org/10.1104/pp.006858
Rymaszewski W, Vile D, Bediee A, Dauzat M, Luchaire N, Kamrowska D, Granier C, Hennig J (2017) Stress-related gene expression reflects morphophysiological responses to water deficit. Plant Physiol 174(3):1913–1930. https://doi.org/10.1104/pp.17.00318
Sales CRG, Ribeiro RV, Silveira JAG, Machado EC, Martins MO, Lagôa AMMA (2013) Superoxide dismutase and ascorbate peroxidase improve the recovery of photosynthesis in sugarcane plants subjected to water deficit and low substrate temperature. Plant Physiol Biochem 73:326–336. https://doi.org/10.1016/j.plaphy.2013.10.012
Sattar A, Sher A, Ijaz M, Ul-Allah S, Rizwan MS, Hussain M, Jabran K, Cheema MA (2020) Terminal drought and heat stress alter physiological and biochemical attributes in flag leaf of bread wheat. PLoS ONE 15(5):e0232974. https://doi.org/10.1371/journal.pone.0232974
Smith AR, Zhao D (2016) Sterility caused by floral organ degeneration and abiotic stresses in Arabidopsis and cereal grains. Front Plant Sci 7:1503. https://doi.org/10.3389/fpls.2016.01503
Stitt M, Hurry V (2002) A plant for all seasons: alterations in photosynthetic carbon metabolism during cold acclimation in Arabidopsis. Curr Opin Plant Biol 5(3):199–206. https://doi.org/10.1016/s1369-5266(02)00258-3
Su Z, Ma X, Guo H, Sukiran NL, Guo B, Assmann SM, Ma H (2013) Flower development under drought stress: morphological and transcriptomic analyses reveal acute responses and long-term acclimation in Arabidopsis. Plant Cell 25(10):3785–3807. https://doi.org/10.1105/tpc.113.115428
Suzuki N, Bassil E, Hamilton JS, Inupakutika MA, Zandalinas SI, Tripathy D, Luo Y, Dion E, Fukui G, Kumazaki A, Nakano R, Rivero RM, Verbeck GF, Azad RK, Blumwald E, Mittler R (2016) ABA is required for plant acclimation to a combination of salt and heat stress. PLoS ONE 11(1):e0147625. https://doi.org/10.1371/journal.pone.0147625
Szécsi J, Joly C, Bordji K, Varaud E, Cock JM, Dumas C, Bendahmane M (2006) BIGPETALp, a bHLH transcription factor is involved in the control of Arabidopsis petal size. EMBO J 25(16):3912–3920. https://doi.org/10.1038/sj.emboj.7601270
Takahashi F, Kuromori T, Urano K, Yamaguchi-Shinozaki K, Shinozaki K (2020) Drought stress responses and resistance in plants: from cellular responses to long-distance intercellular communication. Front Plant Sci 11:556972. https://doi.org/10.3389/fpls.2020.556972
Teotia S, Tang G (2015) To bloom or not to bloom: role of microRNAs in plant flowering. Mol Plant 8(3):359–377. https://doi.org/10.1016/j.molp.2014.12.018
Thalmann M, Santelia D (2017) Starch as a determinant of plant fitness under abiotic stress. New Phytol 214(3):943–951. https://doi.org/10.1111/nph.14491
Turc O, Tardieu F (2018) Drought affects abortion of reproductive organs by exacerbating developmentally driven processes via expansive growth and hydraulics. J Exp Bot 69(13):3245–3254. https://doi.org/10.1093/jxb/ery078
Weaver LM, Amasino RM (2001) Senescence is induced in individually darkened Arabidopsis leaves, but inhibited in whole darkened plants. Plant Physiol 127(3):876–886. https://doi.org/10.1104/pp.010312
Wintermans JFGM, De Mots A (1965) Spectrophotometric characteristics of chlorophylls a and b and their phenophytins in ethanol. Biochim Biophys Acta Biophys Incl Photsynth 109(2):448–453. https://doi.org/10.1016/0926-6585(65)90170-6
Yamaguchi-Shinozaki K, Shinozaki K (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol 57(1):781–803. https://doi.org/10.1146/annurev.arplant.57.032905.105444
Zandalinas SI, Mittler R, Balfagón D, Arbona V, Gómez-Cadenas A (2018) Plant adaptations to the combination of drought and high temperatures. Physiol Plant 162(1):2–12. https://doi.org/10.1111/ppl.12540
Zheng C, Wang Y, Ding Z, Zhao L (2016) Global transcriptional analysis reveals the complex relationship between tea quality, leaf senescence and the responses to cold-drought combined stress in Camellia sinensis. Front Plant Sci 7:1858. https://doi.org/10.3389/fpls.2016.01858
Zhou A, Ma H, Liu E, Jiang T, Feng S, Gong S, Wang J (2017a) Transcriptome sequencing of Dianthus spiculifolius and analysis of the genes involved in responses to combined cold and drought Stress. Int J Mol Sci 18(4):849. https://doi.org/10.3390/ijms18040849
Zhou R, Yu X, Ottosen C-O, Rosenqvist E, Zhao L, Wang Y, Yu W, Zhao T, Wu Z (2017b) Drought stress had a predominant effect over heat stress on three tomato cultivars subjected to combined stress. BMC Plant Biol 17:24. https://doi.org/10.1186/s12870-017-0974-x
Zhou R, Yu X, Zhao T, Ottosen C-O, Rosenqvist E, Wu Z (2019) Physiological analysis and transcriptome sequencing reveal the effects of combined cold and drought on tomato leaf. BMC Plant Biol 19:377. https://doi.org/10.1186/s12870-019-1982-9
Zhou R, Yu X, Ottosen C-O, Zhang T, Wu Z, Zhao T (2020) Unique miRNAs and their targets in tomato leaf responding to combined drought and heat stress. BMC Plant Biol 20:107. https://doi.org/10.1186/s12870-020-2313-x
Zhu J-K (2016) Abiotic stress signaling and responses in plants. Cell 167(2):313–324. https://doi.org/10.1016/j.cell.2016.08.029
Acknowledgements
We would like to thank Prof. AM Tassi for critical revision of the manuscript, and G Caló, M Pérez-Cenci and D Albano for technical assistance.
Funding
This work was funded by grants from the Agencia Nacional de Promoción Científica y Tecnológica (ANPCyT-PICT-2016-0173), the Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET-PIP-2015-11220150100424), and the Universidad Nacional de Mar del Plata (EXA 841/17).
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Fernández Nevyl, S., Battaglia, M.E. Developmental plasticity in Arabidopsis thaliana under combined cold and water deficit stresses during flowering stage. Planta 253, 50 (2021). https://doi.org/10.1007/s00425-021-03575-7
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DOI: https://doi.org/10.1007/s00425-021-03575-7