Agricultural Reviews

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Agricultural Reviews, volume 42 issue 2 (june 2021) : 215-219

Frost Stress Tolerances and Cut Roses: A Review

A.J. Khaskheli1,2, M.I. Khaskheli3, L. Zhang1, A.A. Khaskheli4,*, L.H. Qing1
1Institute of Cell Biology and Ministry of Education Key Laboratory of Cell Activities and Stress Adaptations, School of Life Sciences, Lanzhou University, Lanzhou-730000, China.
2Department of Biotechnology, Faculty of Crop Production, Sindh Agriculture University, Tandojam-70060, Pakistan.
3Department of Plant Protection, Faculty of Crop Protection, Sindh Agriculture University, Tandojam-70060, Pakistan.
4Department of Animal Nutrition, Faculty of Animal Production and Technology, Shaheed Benzair Bhutto University of Veterinary and Animal Sciences, Sakrand, Pakistan.
Cite article:- Khaskheli A.J., Khaskheli M.I., Zhang L., Khaskheli A.A., Qing L.H. (2021). Frost Stress Tolerances and Cut Roses: A Review . Agricultural Reviews. 42(2): 215-219. doi: 10.18805/ag.R-181.
In order to meet the challenges of providing food to the ever increasing population of the world, there is an insistent need to boost crop yield. Unfortunately, the production of agriculture decreasing due to various environmental factors including frost and cold are very important, especially in winter. Indeed, frost is the most important abiotic problem and one of the doctrine limiting factors affecting plant growth and development in winter. Despite various obvious symptoms under frost stress, the yellowing of leaves, weak germination, curling of leaves, decreased rate of cell swelling and wilting, reduced flower opening, curling of petals leads to the cells death. This severe damage is largely due to the sensitive drying associated with freezing during frost. In addition, signal transduction is to switch on frost response genes and transcription factors to mediating stress tolerance, thus underline mechanism of frost stress and genes involve in the frost/cold stress signal network is very important for plant growth and development. In present review, plant significances in daily life and issues related to abiotic stresses such as frost and cold tolerance mechanisms are discussed.

As we all know that, Rose (Rosa hybrida) is one of the most important and economic ornamental plant in the world (Cuizhi and Robertson, 2003). The family of rose (Rosaceae) has been categorized by as an astonishingly large family of flowering plants (Ritz et al., 2005). The flower of this family, which has been characterized by five extricate petals and abundant stamens that jutted as a cup like base structure (Nybon, 2009). In addition, cut roses are one of the most famous and popular flower in the global floral trade. Rose has a deep relationship with human sentiments and has high demand in international markets on account of their use in almost every event (Evans, 2009). However, approximately more than 2,800 species of ornamental roses has been planted around the entire world. Rosa species are found throughout the colder and temperate regions of the northern hemisphere form the arctic to the subtropics (Kim and Janick, 2009). In addition, roses are famous ornamental crops, whether for domestic or commercial cut flowers. Rose plants varies in shape, color and ranging size with compact miniature roses and rose with climbing nature called climbers that can reach a height of a few meters. In addition, significant quantities of flowers are magnificent quality and quantity of rose and other ornamental flowers are grown in most of the steamy and temperate countries of the world (Khan, 2005) and then these flowers needs to transport to far distinct places via ships, or air. At present, there is no comprehensive report has been published regarding the control of frost formation on leaves, flowers and the whole plant surface. Meanwhile, there is no proper attempt have thrive prospectus, but an effort may made to find solution on first observation to authors of this issue. Although the current problem may determine the resistance of plants to frost, it emphasizes the mechanism process, flowering under frost stress, controlling aging and suggesting strategies can solve environmental anxiety problems. Thus, here we are reporting to expand the rose plant in order to have resistance toward the frost stress.   
Existing circumstances of rose in global counties

According to reports, the largest producers of commercial cut flowers are the Netherlands, the United States, Colombia, Kenya, Zimbabwe, Japan and Israel. On the other hand, the total area of ornamental plants produced in these countries is 223,145 hectares. Cut flowers are the leader in ornamental plants with total sales of $24.7 billion (Kndirli and Cakmak, 2007). Despite this, Rose is the most important ornamental plant in the world. At the Chinese and Nonetheless, Roses are also the most important ornamental plants worldwide and cut roses account for about 21% and 31% of all cut flowers traded in China and at the European auctions respectively (Heinrichs, 2008). Commercially, roses are usually harvested during the open germination and are highly susceptible to WDS during post-harvest handling. WDS causes abnormal flowers to open, flowers wilted, pedicels (bent neck) atrophy and inability to open (Jin et al., 2006; Xue et al., 2008). Therefore, the effects of dehydration on the opening and senescence of cut rose roses have been studied at physiological and biochemical levels for decades (Kumar and Srivastaya 2008).

Transcriptional factors trigger or repress the expression of defense gene
Morphological changes that occur during flower opening usually include the growth and expansion of the petals, which is also important for rose flowers. The growth of petals is a complex process that integrates cell division and cell expansion. Like Arabidopsis thaliana, cell division is usually phased out in petals before bud opening and flower development and cell expansion promotes petal growth primarily in later stages. Similarly, in roses, the growth of petals depends to a large extent on the cell expansion in the late stages of flower opening. Ethylene is usually produced by higher plants associated with fruit ripening and specific triple reactions. Often, various biotic and abiotic stresses, including temperature fluctuations, water imbalances, salinity, pathogens or insect infestation, can have some specific types of negative effects on plant growth and development. On this issue of concern, nature always manifests itself in an adoptive way. In these circumstances, plants adopt various defense mechanisms to sense the stimulation of the surrounding environment. Transcription factors are known for their critical function of triggering or inhibiting defense gene expression during signal transduction and for the regulation of connectivity between various signaling pathways (Evans, 2009).
It has been observed that the ERF gene is not only stimulated by disease-related and pathogen infection stimulation, but also trigger the expression level on abiotic stresses. Therefore, ERF genes such as RhERF can improve the multiple stress resistance of transgenic plants. In addition, analysis of the overexpression of ERF genes indicates that these transcription factors can confer broad-spectrum resistance to pathogens and other abiotic stresses and can also make transgenic plants resistant to drought, salt and freezing. Therefore, the RhERF gene might be focus for specific research to explore the role of plant development in relation to abiotic stress tolerance (ethylene stimulation).
Progression of frost resistance plant
Various frost resistance mechanisms have evolved in alpine woody plants. In addition to enduring the presence of ice on tissues and the accompanying dehydration stress, some tissues and organs that depend on avoiding freezing (Gilbert, 2014). In many species, the mechanism by which they survive at freezing temperatures is unclear and therefore represents fertile ground for future research. In cold weather conditions, frost falls on plants and can cause significant damage. Agriculture suffers severe losses each year due to frost-damaged crops (Ladinig et al., 2013). Researchers hope that spraying ice-borne bacteria on a wide variety of plants can help to avoid annual damage caused by frost conditions. Negative ice bacteria are a common mutant of the wild type P. syringae. In addition, wild-type P. syringae bacteria are known as ice-suppressing bacteria. It contains a surface protein in its outer wall that helps to form frost, hence the name “ice +” (Kumar et al., 2008). In case of mutant Pseudomonas syringae, there is a lack of surface proteins that promote ointment, so these types of bacteria cannot promote the formation of frost and are therefore called as negative ice bacteria (Hirano and Upper, 2000). Both negative ice bacteria and ice plus bacteria are found in nature. However, spraying of negative ice bacteria on crops have been mass-produced using recombinant DNA technology. While, Prasanth et al., (2015) reported that the discovery of this bacterium was in the 1970s, when Dr. Lindow discovered that a specific bacterium isolated from dry leaf powder of frozen damaged plants  introduced into plants that did not exist, these plants become very vulnerable to frost damage. He further continued to identify the bacterium as Pseudomonas syringae, the role of P. syringae in the ice nucleus and in 1977 discovered a mutant negative ice strain. The negative ice strain of P. syringae was also successfully developed by recombinant DNA technology. But now we can consider the recombinant Pseudomonas syringae (Ice in minus) as one of the most successful microorganisms introduced into the environment. The ice minus is the generic name for a strain of Pseudomonas syringae, which lacks the ability to produce surface proteins. Most wild-type strains of P. syringae are “ice plus”, have the ability to produce proteins found on the outer cell wall of bacteria and act as a nucleation center for ice crystals. The ice-minus variant of P. syringae is a mutant, lacking the gene responsible for ice-nucleating surface protein production. The lack of surface proteins provides a more unfavorable environment for the formation of ice. Both strains of P. syringae are naturally occurring. Sometimes water is mixed with the ice-nucleated active protein of P. syringae bacteria. These proteins act as effective nuclei, triggering the formation of ice crystals at relatively high temperatures, so the droplets will turn into ice before falling to the ground. However, frost at the time of flowering delays maturity but only leads to a small decline in yield production (Chinnusamy et al., 2003).

Frost after flowering can lead to a sharp drop in production and a decline in grade loss. Frost during flowering usually causes abortion of flowers. The researchers observed that only the flowers that were opened during the frost were affected by the plants. The pods descend on the stem and the unopened buds continue to develop normally. A few days after the frost, the gap between the pods of the abortion was clearly visible on the stem. The damage is obvious because all open flowers show signs of damage during frost (Ladinig et al., 2013).
Genes regulation of frost resistances
Recent advances in the fields of biotechnology and genetic engineering offer new strategies for the development of mutant plants that are more tolerant to cold stress. The rapid development of recombinant DNA technology and the development of precise and efficient gene transfer protocols have led to efficient transformation of many crop species and the production of transgenic lines (Wani et al., 2008; Wani and Gosal, 2011). Many genes that respond to freezing stress have been isolated and characterized. Many studies have shown that the expression of cold regulatory genes is critical for cold tolerance in plants (Knight et al., 1999; Tamminen et al., 2001; Hsieh et al., 2002). In addition, many reported studies demonstrate the sensation of mutation methods in promoting tolerance to low temperature stress. At the same time, Kenji and Tsuyoshi (2013) reviewed the citations and reported the cold tolerance of many cold-stressed host genes in different species, such as the chloroplast GPAT (glycerol 3-phosphate acyltransferase) of pumpkin, the largest genus of Cucurbita and Arabidopsis. The unsaturation of fatty acids in phosphatidylglycerols increases the ratio of unsaturated fatty acids in plant cell membranes, thereby increasing cold tolerance (Murata et al., 1992). The citrus LEA gene CuCOR19 enhances the cold tolerance of transgenic tobacco (Hara et al., 2003). Similarly, the expression of the wheat dehydrin WCS19 (Danyluk et al., 2002), Arabidopsis COR15A (Artus et al., 1996) and the coexpression of RAB18 and CO47 or LTI29/XERO2 and LTI30/ERD10 (Puhakainen et al., 2004) improved the proposed freeze resistance of Arabidopsis transgenic plants. The freeze-tolerance of transgenic strawberry leaves expressing wheat dehydrin WCO410 was improved. Overexpression of rice TPP1 (trehalose 6-phosphate phosphatase) enhances cold tolerance in rice (Ge et al., 2008). Since trehalose is a non-reducing disaccharide that acts as a stress-protecting metabolite, the accumulation of trehalose enhances cold tolerance and other abiotic stresses (Jang et al., 2003). These results indicate that defense genes play an important role in plant response to low temperatures.

Fig 1: Frost stress tolerances regulating genes.


Fig 2: Gene regulation modulating stress response and tolerances.

Low temperature stresses are the major environmental factor that not only limit where crops can be grown but also reduces yields depending on the weather in a particular growing season. Except for years of extreme stress, which can lead to a sharp drop in production, it is almost certain that extreme pressures are small and it is almost certain that losses in large areas are small and produce comparable production declines each year. To meet future global food needs, crop yields must be increased in challenging environments. With conventional breeding, it is difficult to produce complete and timely resistance to biotic and abiotic stresses. In addition, analysis of overexpression of ERF genes indicates that these transcription factors can confer broad-spectrum resistance to pathogens and other abiotic stresses and can also make transgenic plants resistant to drought, salinity and freezing.        

Often, various biotic and abiotic stresses, including temperature fluctuations, water imbalances, salinity, pathogens or insect infestation, can have some specific types of negative effects on plant growth and development. On this issue of concern, nature always manifests itself in an adoptive way. In these circumstances or internal hints, plants adopt various defense mechanisms to sense the stimulation of the surrounding environment and then change it. Transcription factors are known for their critical function of triggering or inhibiting defense gene expression in signal transduction and for the regulation of connectivity between various signaling pathways (Ge et al., 2008). It has been observed that the ERF gene is not only stimulated by disease-related and pathogen infection stimulation, but also because abiotic stress can trigger its expression level. Therefore, ERF genes such as RhERF can improve the multiple stress resistance of transgenic plants. Therefore, various challenges should be noted in terms of cold pressure. As noted above, low temperature sensation is believed to involve various major aspects and each sensor can sense a particular aspect of stress. Elucidating the regulatory and signaling mechanisms of cold stress is an important goal to gain a complete understanding of the cold signaling mechanism.

I would like to thank School of Life Sciences, Lanzhou University, Gansu Province, P.R. China for providing me an opportunity for Post doctorate program and able to proceed this manuscript. I also thankful to the Department of Biotechnology, Sindh Agriculture University, Tandojam, Pakistan for provided me a platform to teach, guide and supervise the students and facilitated the highly prospectus educations for the newly brilliant students.

  1. Artus, N.N., Uemura, M., Steponkus, P.L., Gilmour, S.J., Lin, C. and Thomashow, M.F. (1996). Constitutive expression of the cold-regulated Arabidopsis thaliana COR15a gene affects both chloroplast and protoplast freezing tolerance. Proceedings of National Academy of Science. 93: 13404-13409.

  2. Chinnusamy, V., Kanrar, M.O., Lee, B.H., Hong, X., Agarwal, M. and Zhu, J.K. (2003). ICE1: a regulator of cold-induced transcriptome and freezing tolerance in Arabidopsis. Genetics Development. 17: 1043-1054.

  3. Cuizhi, G. and Robertson, K.R. (2003). Rosa Linnaeus, Sp. Flora of China. 9: 339-381.

  4. Danyluk, J., Wilson, K.E., Pocock, T., Huner, N.P. and Sarhan, F. (2002). Cold-regulated cereal chloroplast late embryogenesis abundant-like proteins. Plant Physiology. 129: 1368-1381.

  5. Evans, A. (2009). Rose imports. Floraculture International Feb. 2009. pp. 42-43.

  6. Ge, L.F., Chao, D.Y., Shi, M., Zhu, M.Z., Gao, J.P. and Lin, H.X. (2008). Overexpression of the trehalose-6-phosphate phosphatase gene OsTPP1 confers stress tolerance in rice and results in the activation of stress responsive genes. Planta. 228: 191-201.

  7. Gilbert, N. (2014). Frost resistance in alpine woody plants. Frontiers in Plant Science. 5: 654-662.

  8. Hara, M., Terashima, S., Fukaya, T. and Kuboi, T. (2003). Enhancement of cold tolerance and inhibition of lipid peroxidation by citrus dehydrin in transgenic tobacco. Planta. 217: 290-298.

  9. Heinrichs, F. (2008). International Statistics Flowers and Plants. AIPH/Union Fleurs. 56:16-90.

  10. Hirano, S.S. and Upper, C.D. (2000). Bacteria in the Leaf Ecosystem with Emphasis on Pseudomonas syringae-a Pathogen, Ice Nucleus and Epiphyte. Microbiology and Molecular Biology Reviews. 64(3): 624-653.

  11. Hsieh, T.H., Lee, J.T., Yang, P.T., Chiu, L.H., Charng, Y.Y., Wang, Y.C. and Chan, M.T. (2002). Heterology expression of the Arabidopsis C-repeat/dehydration response element binding factor 1 gene confers elevated tolerance to chilling and oxidative stresses in transgenic tomato. Plant Physiology. 129(3): 1086-1094.

  12. Jang, I.C., Oh, S.J., Seo, J.S., Choi, W.B., Song, S.I., Kim, C.H., Kim, Y.S., Seo, H.S., Choi, Y.D. and Nahm, B.H. (2003). Expression of a bifunctional fusion of the Escherichia coli genes for trehalose-6-phosphate synthase and trehalose-6-phosphate phosphatase in transgenic rice plants increases trehalose accumulation and abiotic stress tolerance without stunting growth. Plant Physiology. 131: 516-524.

  13. Jin, J.S., Shan, N.W., Ma, N., Bai, J.H. Gao, J.P. (2006). Regulation of ascorbate peroxidase at the transcript level is involved in tolerance to postharvest water deficit stress in the cut rose (Rosa hybrida L.) cv. Samantha. Postharvest Biological Technology. 40: 236-243.

  14. Kenji, M. and Tsuyoshi, F. (2013). Cold signaling and cold response in plants. International Journal of Molecular Science. 14: 5312-5337.

  15. Khan, M.A. (2005). Development of commercial floriculture in Asia and Pacific: Issues, challenges and opportunities. Proceedings of national saminar on streamlining production and export of cut flowers and house plants. (Ed.): Hort. Foundation Pak. 2nd-4th March. pp. 36.

  16. Kim, E.H. and Janick, J. (2009). Genetics and Genomics of osaceae. Plant Genetics and Genomics: Crops and Models. 33: 232-244.

  17. Kndirli, B. and Cakmak, B. (2007). Economics of cut flower production in greenhouses: Case study from Turkey. Agriculture Journal. 2(4): 499-502.

  18. Knight, H., Veale, E.L., Warren, G.J. and Knight, M.R. (1999). The sfr6 mutation in Arabidopsis suppresses low-temperature induction of genes dependent on the CRT/DRE sequence motif. Plant Cell: 11(5): 875-86

  19. Kumar, N., Srivastava, G.C. and Dixit, K. (2008). Flower bud opening and senescence in roses (Rosa hybrida L.). Plant Growth Regulation. 55: 81-99.

  20. Ladinig, U., Hacker, J., Neuner, G. and Wagner, J. (2013). How endangered is sexual reproduction of high-mountain plants by summer frosts? Frost resistance, frequency of frost events and risk assessment. Oecologia. 171: 743-760. 

  21. Murata, N., Ishizaki-Nishizawa, O., Higashi, S., Hayashi, H., Tasaka, Y. and Nishida, I. (1992). Genetically engineered alteration in the chilling sensitivity of plants. Nature. 356: 710-713.

  22. Nybon, H. (2009). Introduction to Rosa. In: Plant Genetics and Genomics: Genetics and Genomics of Rosaceae, Crops and Models 6, [(Eds.) Folta, K.M. and Gardiner, S.E.] Springer Science Business Media LLC., pp: 339-351.

  23. Prasanth, M, Ramesh, N., Gothandam, K.M., Sivamangala, K. and Shanthin, M. (2015). Pseudomonas Syringae: An Overview and its future as a “Rain Making Bacteria” i T. School of Bio Sciences and Technology, VIT University Vellore, Tamil Nadu, India. International Research Journal of Biological Science. 4(2): 70-77. 

  24. Puhakainen, T., Hess, M.W., Makela, P., Svensson, J., Heino, P. and Palva, E.T. (2004). Overexpression of multiple dehydrin genes enhances tolerance to freezing stress in Arabidopsis. Plant Molecular Biology. 54: 743-753.

  25. Ritz, C.M., Schmuths, H. and Wissemann, V. (2005). Evolution by reticulation: European dogroses originated by multiple hybridization across the genus of Rosa. Journal of Heredity. 96(1): 4-14.

  26. Tamminen I., Mäkelä, P., Heino, P. and Palva, E.T. (2001). Ectopic expression of ABI3 gene enhances freezing tolerance in response to abscisic acid and low temperature in Arabidopsis thaliana. Plant Journal. 25(1): 1-8.

  27. Wani S.H., Sandhu, J.S. and Gosal, S.S. (2008). Genetic engineering of crop plants for abiotic stress tolerance, Advanced Topics in Plant Biotechnology and Plant Biology. New Delhi: MD Publications; pp. 149-183.

  28. Wani, S.H. and Gosal, S.S. (2011). Introduction of OsglyII gene into Indica rice through particle bombardment for increased salinity tolerance. Biological Plant. 11: 102-112.

  29. Xue, J.Q., Li, Y.H., Tan, H., Yang, F., Ma, N. and Gao, J.P. (2008). Expression of ethylene biosynthetic and receptor genes in rose floral tissues during ethylene-enhanced flower opening. Journal of Experimental Botany. 8: 2161-2169.

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