Abstract
Cold stress is an important factor limiting the growth and distribution of pineapple. Breeding cold-resistant germplasm is an effective way to cope with this problem. In vitro selection for the somaclonal variation using different selection agents has been used for crop improvement in stress tolerance. In this study, the pineapple cold-tolerant variant was developed through in vitro cold selection of somaclonal variations. Low temperature was used as the selected agent, and the extreme lethal condition for the in vitro pineapple cultures was determined to be 0 °C for 72 h. The morphology changes of the in vitro cultures during the cold selection were observed and analyzed. The cold-tolerant variant line was finally obtained through three consecutive selections with cold shock treatments, based on the established high-efficiency culture system for pineapple embryogenic calli. The genetic variations at the molecular level in the cold-tolerant variant were verified by ISSR analysis. The significantly improved cold tolerance in our selected variant was mainly reflected by the higher survival rate, increased proline content, and elevated SOD activity under cold stress compared to these qualities in the control plants. This study demonstrated the feasibility of in vitro selection for cold tolerance in pineapple. The cold-tolerant variant could be valuable for future pineapple breeding programs and for cold tolerance research.
Similar content being viewed by others
References
Anis M, Ahmad N (2016) Plant tissue culture: propagation, conservation and crop improvement. Springer, Singapore
Anwar A, Kikuchi A, Watanabe KN (2010) Assessment of somaclonal variation for salinity tolerance in sweet potato regenerated plants. Afr J Biotechnol 9:7256–7265
Ashrafzadeh S, Leung DMW (2015) In vitro breeding of heavy metal-resistant plants: a review. Hortic Environ Biote 56:131–136
Bairu MW, Aremu AO, Van Staden J (2010) Somaclonal variation in plants: causes and detection methods. Plant Growth Regul 63:147–173
Baker CJ, Mock NM (1994) An improved method for monitoring cell death in cell suspension and leaf disc assays using evans blue. Plant Cell Tissue Organ Cult 39:7–12
Bartholomew DP, Paull RE, Rohrbach KG (2002) The pineapple: botany, production, and uses. CABI
Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207
Bertin P, Bouharmont J (1997) Use of somaclonal variation and in vitro selection for chilling tolerance improvement in rice. Euphytica 96:135–142
Caboni E, Anselmi S, Donato E, Manes F (2003) In vitro selection of Actinidia deliciosa clones tolerance to NaCl and their molecular and in vivo ecophysiological characterisation. Acta Hortic 618:77–83
Carloni E, Tommasino E, Colomba EL, Ribotta A, Quiroga M, Griffa S, Grunberg K (2017) In vitro selection and characterization of buffelgrass somaclones with different responses to water stress. Plant Cell Tissue Organ Cult 130:265–277
Chen L, Xiang H, Miao Y, Zhang L, Guo Z, Zhao X, Lin J, Li T (2014a) An overview of cold resistance in plants. J Argon Crop Sci 200:237–245
Chen Y, Jiang J, Chang Q, Gu C, Song A, Chen S, Dong B, Chen F (2014b) Cold acclimation induces freezing tolerance via antioxidative enzymes, proline metabolism and gene expression changes in two chrysanthemum species. Mol Biol Rep 41:815–822
Chen C, Zhang Y, Xu Z, Luan A, Mao Q, Feng J, Xie T, Gong X, Wang X, Chen H, He Y (2016) Transcriptome profiling of the pineapple under low temperature to facilitate its breeding for cold tolerance. PLoS ONE 11:e0163315
Dhurve L, Ajith Kumar K, Bhaskar J, Sobhana A, Francies RM, Mathew D (2021) Wide variability among the ‘Mauritius’ somaclones demonstrates somaclonal variation as a promising improvement strategy in pineapple (Ananas comosus L.). Plant Cell Tissue Organ Cult 145:701–705
Dix PJ (1993) The role of mutant cell lines in studies on environmental stress tolerance: an assessment. Plant J 3:309–313
Dong HL, Lee CB (2000) Chilling stress-induced changes of antioxidant enzymes in the leaves of cucumber: in gel enzyme activity assays. Plant Sci 159:75
Dörffling K, Dörffling H, Lesselich G (1993) In vitro-Selection and regeneration of hydroxyproline-resistant lines of winter wheat with increased proline content and increased frost tolerance. J Plant Physiol 142:222–225
Duncan DR, Widholm JM (1987) Proline accumulation and its implication in cold tolerance of regenerable maize callus. Plant Physiol 83:703
Efferth T (2019) Biotechnology applications of plant callus cultures. Engineering 5:50–59
Frascaroli E (2018) Breeding cold-tolerant crops. In: Wani SH (ed) Cold tolerance in plants, 1st edn. Springer, Cham, pp 159–177
Ge H, Li Y, Fu H, Long G, Luo L, Li R, Deng Z (2015) Production of sweet orange somaclones tolerant to citrus canker disease by in vitro mutagenesis with EMS. Plant Cell Tissue Organ Cult 123:29–38
Giannopolitis CN, Ries SK (1977) Superoxide dismutases: I. Occurrence in Higher Plants Plant Physiol 59:309–314
Gosal SS, Kang MS (2012) Plant tissue culture and genetic transformation for crop improvement. Wiley, Hoboken
Halim NAA, Tan BC, Midin MR, Madon M, Khalid N, Yaacob JS (2018) Abscisic acid and salinity stress induced somaclonal variation and increased histone deacetylase (HDAC) activity in Ananas comosus var. MD2. Plant Cell Tissue Organ Cult 133:123–135
Hammerschlag FA (2000) Resistant responses of peach somaclone 122–1 to Xanthomonas campestris pv. pruni and to Pseudomonas syringae pv. syringae. HortScience 35:141–143
He YH, Luo J, Hu ZY, Wang RX, Gao AP, Zhao CX, Yang XH, Ye ZX, Wang ZH (2008) Classification and organogenesis of non-embryogenic callus from Ananas comosus. J Fruit Sci 25:65–68
He YH, Fang SQ, Ma J, Hu ZY, Lu M, Peng B (2010) Histocytology observation on the somatic embryogenesis in Ananas comosus callus. Acta Horticult Sin 37:689–696
He YH, Fang SQ, Hu ZY, Ma J, Luo J, Wu CH, Cao L, Lu M, Chen CJ (2012) Morphological and Anatomical analysis of pineapple somatic embryogenesis. Acta Horticult Sin 39:57–63
Hwang SC, Ko WH (2004) Cavendish banana cultivars resistant to Fusarium wilt acquired through somaclonal variation in Taiwan. Plant Dis 88:580–588
Jain SM, Brar DS, Ahloowalia BSE (2013) Somaclonal variation and induced mutations in crop improvement, vol 32. Springer, New York
Koç İ, Akdemir H, Onay A, Çiftçi YÖ (2014) Cold-induced genetic instability in micropropagated Pistacia lentiscus L. plantlets. Acta Physiol Plant 36:2373–2384
Kohpaii FN, Farahani F, Noormohammadi Z (2017) Somaclonal variation in the in vitro regenerated pineapple (Ananas comosus): investigation of the cellular characteristics biochemical specificities and ISSR markers. Phytol Balc 23:73–83
Krishna H, Alizadeh M, Singh D, Singh U, Chauhan N, Eftekhari M, Sadh RK (2016) Somaclonal variations and their applications in horticultural crops improvement. 3 Biotech 6:1–18
Kuksova VB, Piven NM, Gleba YY (1997) Plant cell variation and in vitro induced mutagenesis in grapevine. Plant Cell Tissue Organ Cult 49:17–27
Li R, Qu R, Bruneau AH, Livingston DP (2010) Selection for freezing tolerance in St. Augustinegrass through somaclonal variation and germplasm evaluation. Plant Breed 129:417–421
Liu J, Yang Z, Li W, Yu J, Huang B (2013) Improving cold tolerance through in vitro selection for somaclonal variations in Seashore paspalum. J Am Soc Hortic Sci 138:452–460
Liu MY, Sun J, Wang KY, Liu D, Li ZY, Zhang J (2014) Spermidine enhances waterlogging tolerance via regulation of antioxidant defence, heat shock protein expression and plasma membrane H+-ATPase activity in Zea mays. J Argon Crop Sci 200:199–211
Lobo MG, Paull RE (2017) Handbook of pineapple technology: postharvest science, processing and nutrition. Wiley, Hoboken
Lu XH, Sun DQ, Ye CH, Li YZ, Sun GM (2010) Growth, physiological characteristics and evaluation of cold tolerance of pineapple seedlings under low temperature stress. Acta Bot Boreali Occident Sin 30:2054–2060
Luan A, He Y, Xie T, Chen CJ, Mao Q, Wang X, Li C, Ding Y, Lin W, Liu C, Xia J, He J (2019) Identification of an embryonic cell-specific region within the pineapple SERK1 promoter. Genes 10:883
Ma J, He Y, Wu C, Liu H, Hu Z, Sun G (2011) Cloning and Molecular characterization of a SERK gene transcriptionally induced during somatic embryogenesis in Ananas comosus cv. Shenwan. Plant Mol Biol Rep 30:195–203
Maleki M, Ghorbanpour M, Nikabadi S, Wani SH (2019) In vitro screening of crop plants for abiotic stress tolerance. In: Wani S (ed) recent approaches in omics for plant resilience to climate change. Springer, Cham, pp 75–91
Montero-Calderón M, Cerdas-Araya MDM (2012) Tropical and subtropical fruits: postharvest physiology, processing and packaging. Wiley, Hoboken
Nacheva LR, Gercheva PS, Andonova MY, Panayotova DV, Dzhuvinov VT (2014) Somaclonal variation: a useful tool to improve disease resistance of pear rootstock ‘Old Home 9 Farmingdale’(OHF 333) (Pyrus communis L.). Acta Hortic 1056:253–258
Ogata T, Yamanaka S, Shoda M, Urasaki N, Yamamoto T (2016) Current status of tropical fruit breeding and genetics for three tropical fruit species cultivated in Japan: pineapple, mango, and papaya. Breed Sci 66:69–81
Pérez G, Mbogholi A, Sagarra F, Aragón C, González J, Isidrón M, Lorenzo JC (2011) Morphological and physiological characterization of two new pineapple somaclones derived from in vitro culture. In Vitro Cell Dev Plant 47:428–433
Pérez G, Yanez E, Mbogholi A, Valle B, Sagarra F, Yabor L, Aragón C, González J, Isidrón M, Lorenzo JC (2012) New pineapple somaclonal variants: P3R5 and Dwarf. Am J Plant Sci 03:1–11
Py C, Lacoeuilhe JJ, Teisson C (1987) The pineapple cultivation and uses. G-P Maisonneuve & Larose, Pairs
Rai MK, Kalia RK, Singh R, Gangola MP, Dhawan AK (2011) Developing stress tolerant plants through in vitro selection: an overview of the recent progress. Environ Exp Bot 71:89–98
Sanewski GM (2018) The history of pineapple improvement, genetics and genomics of pineapple. Springer, Cham
Sengar AS, Thind KS, Kumar B, Pallavi M, Gosal SS (2009) In vitro selection at cellular level for red rot resistance in sugarcane Saccharum sp. Plant Growth Regul 58:201–209
Shi H, Huang R, Liu Y, Chen X, Lu S, Guo Z (2020) Identification of a cold tolerant mutant in seashore paspalum (Paspalum vaginatum). Plant Cell Tiss Organ Cult 140:379–387
Siddique I (2020) Propagation and genetic manipulation of plants. Springer, Singapore
Silva RLD, Ferreira CF, Ledo CADS, Souza EHD, Silva PHD, Souza FVD (2016) Viability and genetic stability of pineapple germplasm after 10 years of in vitro conservation. Plant Cell Tiss Organ Cult 127:123–133
Smith MK, Botella JR (2020) Ananas comosus pineapple. In: Richard EL (ed) Biotechnology of fruit and nut crops, 2nd edn. CABI, Boston, pp 118–130
Sripaoraya S, Marchant R, Power JB, Davey MR (2003) Plant regeneration by somatic embryogenesis and organogenesis in commercial pineapple (Ananas comosus L.). In Vitro Cell Dev Plant 39:450–454
Steponkus PL, Lanphear FO (1967) Refinement of the triphenyl tetrazolium chloride method of determining cold injury. Plant Physiol 42:1423
Tal M (1994) In vitro selection for salt tolerance in crop plants: Theoretical and practical considerations. In Vitro Plant 30:175–180
Tricker P, Trewin HO, Clarkson G, Eensalu E, Tallis M, Colella A, Doncaster C, Sabatti M, Taylor G (2005) Stomatal conductance and not stomatal density determines the long-term reduction in leaf transpiration of poplar in elevated CO2. Oecologia 143:652–660
Turk H, Erdal S, Genisel M, Atici O, Demir Y, Yanmis D (2014) The regulatory effect of melatonin on physiological, biochemical and molecular parameters in cold-stressed wheat seedlings. Plant Growth Regul 74:139–152
Vanijajiva O (2012) Assessment of genetic diversity and relationships in pineapple cultivars from Thailand using ISSR marker. Int J Agric Technol 8:1829–1838
Verma D, Ansari MW, Agrawal GK, Rakwal R, Shukla A, Tuteja N (2013) In vitro selection and field responses of somaclonal variant plants of rice cv PR113 for drought tolerance. Plant Signal Behav 8:e23519
Wang SM, Lan H, Jia HH, Xie KD, Wu XM, Chen CL, Guo WW (2016) Induction of parthenogenetic haploid plants using gamma irradiated pollens in ‘Hirado Buntan’ pummelo (Citrus grandis [L.] Osbeck). Sci Hortic-Amsterdam 207:233–239
Whitehouse AB, Johnson AW, Passey AJ, McLeary KJ, Simpson DW (2014) Serenity’: a paler skin-coloured somaclonal variant of the short-day cultivar ‘Florence. Acta Hortic 1049:819–821
Funding
This work was funded by National Natural Science Foundation of China (31801831), National Key Research and Development Project (2019YFD1000505, 2018YFD10005000).
Author information
Authors and Affiliations
Contributions
CYL and YHH conceived and designed the experiments; YFZ, ZQX, WZ performed the experiments; TX and YFZ analyzed the data; ZQX and WZ contributed reagents and materials; CYL and YHH wrote the paper.
Corresponding authors
Ethics declarations
Conflict of interest
There is no conflict of interest between the authors.
Additional information
Communicated by Ali Sarkhosh.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Zhang, Y., Xu, Z., Xie, T. et al. In vitro selection and identification of a cold-tolerant variant in pineapple (Ananas comosus). Hortic. Environ. Biotechnol. 63, 275–286 (2022). https://doi.org/10.1007/s13580-021-00396-1
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13580-021-00396-1