Transgenic herbicide-resistant turfgrasses
1. Introduction
Turfgrasses grow in different habitats for numerous purposes worldwide. They are cultivated for their agronomical, environmental, ornamental, recreational and stock feeding values [1, 2]. Various turfgrasses are used for environmental beautification and for the protection of resources such as land, soil and water. Many varieties of turfgrasses cover home yards, golf courses, parks, soccer fields, and roadsides, etc. To cite a few examples of renewed interest in turfgrasses, they play a significant environmental role in photosynthetically fixing carbon dioxide to evolve oxygen into the atmosphere. In addition to their vast acreage of widespread forage, planting of the grasses in urban areas such as rooftops, parks and, more recently automobile parking lots, contributes to the suppression of urban heat island phenomena [3]. Various causes of soil erosion and losses due to flood washout and landslide can also be circumvented and managed, as the damages are greatly reduced and the conservation of soil moisture and underground water is effectively sustained by the planting of turfgrass varieties. Recreational and sporting activities on the natural turfgrass field, compared to an artificial turf, greatly reduce the risk of personal injuries, thus contributing to the wellbeing of people in general.
Not surprisingly, the worldwide turfgrass market and its associated herbicide sales are substantial; in the United States alone, turfgrass is one of the four major staple crops, second only to corn [4, 5]. In facing the challenge of global warming, turfgrasses are gaining attention of both environmentalists and agronomists for their role in the certified emission reductions. Relatively high production costs of cultivating and maintaining turfgrasses concerns them, however. Healthy swarth growth and well-maintained turf habitats entail herbicide spraying because otherwise dominant weed varieties easily overtake the sward. Annually, their maintenance costs alone run around 4.5 billion dollars in the United States [4, 6]. One of the major costs is certainly herbicidal requirement.
Herbicidal agrochemicals are classified into two categories, selective and non-selective herbicides. The latter kills all plant species, whereas the former is targeted at specific plant(s)/weed(s) for herbicidal action. The biochemical mechanisms of herbicides include the disruptions of (i) the photosynthesis by blocking the photosynthetic reaction centers, electron transport system or photo-oxidative membrane damages, (ii) cell division and root development, (iii) energy transduction and metabolism, (iv) plant growth hormones, (v) biosynthesis of amino acids/proteins and (vi) disruption of other physiologically significant molecules such as chlorophylls and carotenoids, as discussed elsewhere in this volume.
Frequent herbicide applications also pose serious environmental and health concerns, for example, to the authors’ residential island of Jeju where there are 30 golf courses open for business. In spite of the current difficulties arising from the public objections, genetically modified turfgrasses with a herbicide-resistant gene provide an effective alternative to the wide applications of agrochemical herbicides. Since the development and ecological impact studies of transgenic herbicide-resistant creeping bentgrass [7, 8] and zoysiagrass [9, 10], several GM varieties of turfgrasses including those of herbicide-resistant cultivars have been developed (see Table 1). Most recently, in reference [11] bentgrass ASR-368 has been patented for its commercial rights. With an increasing number of reports on transgenic herbicide-resistant turfgrasses, it is appropriate to review the subject at this time. Discussion in this chapter focuses on the transgenic herbicide-resistant turfgrasses developed primarily in our laboratory here in Jeju and Gwangju, Korea. For a review of other transgenic grasses with herbicide-resistance traits, see Table 1 and references therein.
|
|
|
|
|
|
|
|
|
Crenshaw |
|
|
|
Disease resistance | [16] | |
Crenshaw |
|
|
|
Drought tolerance | [33] | ||
Crenshaw |
|
|
|
Herbicide resistance/Disease resistance | [34] | ||
Crenshaw |
|
|
|
Purple-color | [35] | ||
Crenshaw |
|
|
|
Herbicide resistance/Drought tolerance/dwarf | [36] | ||
Crenshaw, Penncross |
|
|
bar | Herbicide resistance | [37] | ||
Penncross | Electroporation |
|
|
Herbicide resistance | [38] | ||
Penncross | Electroporation |
|
|
Herbicide resistance | [39] | ||
Penncross |
|
|
|
Drought/salt tolerance | [40] | ||
Penncross |
|
|
|
Herbicide resistance | [22] | ||
Penncross |
|
|
|
Herbicide resistance/dwarf | [41] | ||
Province Penn-A-4 | Biolistics |
|
|
Herbicide resistance/Disease resistance | [42] | ||
Penn-A-4 |
|
|
bar | Herbicide resistance | [43] | ||
Penn-A-4 |
|
|
|
Herbicide resistance/Disease resistance | [44] | ||
Penn-A-4 |
|
|
|
Herbicide resistance/Salt tolerance | [45] | ||
|
Suthshore Emerald |
Biolistics |
|
|
Herbicide resistance | [46] | |
Regent Tiger |
|
|
|
Herbicide resistance | [47] | ||
Cobra | Electroporation |
|
|
Herbicide resistance | [48] | ||
Biolistics |
|
|
Herbicide resistance | [49] | |||
|
TifEagle | Biolistics |
|
|
Herbicide resistance | [50] | |
TifEagle |
|
|
|
Herbicide resistance | [51] | ||
|
Embryogen-P | Biolistics |
|
|
Herbicide resistance | [52] | |
Rapido | Biolistics |
|
|
Herbicide resistance | [53] | ||
|
Protoplasts |
|
|
Herbicide resistance | [54] | ||
Alley | Biolistics |
|
|
Herbicide resistance/ Cole tolerance | [55] | ||
|
Protoplasts |
|
|
Herbicide resistance | [56] | ||
|
Riikka | Biolistics |
|
|
Herbicide resistance/ Freezing tolerance | [57] | |
TopGun |
|
|
|
Herbicide resistance/ Salt tolerance | [58] | ||
|
Alamo | Biolistics |
|
|
Herbicide resistance | [59] | |
Alamo |
|
|
|
Herbicide resistance | [60] | ||
|
Tifton-7 | Biolistics |
|
|
Herbicide resistance | [61] | |
Pensacola | Biolistics |
|
|
Herbicide resistance | [62] | ||
|
|
|
|
Herbicide resistance | [63] | ||
|
|
|
|
Herbicide resistance | [15] | ||
Zenith | Biolistics |
|
|
Herbicide resistance | [64] | ||
|
|
|
Herbicide resistance/ Shade tolerance | [10] | |||
|
|
|
|
Herbicide resistance/ Chilling tolerance | [65] |
2. Turfgrass species
There are some 7,500 turfgrass species of more than 600 genera distributed worldwide. Of these, 30~40 species are cultivated as agronomic plants [1]. Turfgrasses are generally classified into two major species, warm and cold season grasses. The plants are also divided into two groups based on their mechanism of photosynthetic carbon dioxide fixation, C3 and C4 plants. As representative C4 warm season turfgrasses with optimal growth temperatures of 27~35°C, zoysiagrass and Bermuda grass species are widely used for sports fields because of their strong traits such as swarth growth, vegetative propagation and drought tolerance as they are cultivated widely, especially in China, Japan and Korea. However, they tend to grow relatively slowly and particularly with zoysiagrasses prematurely lose their greenness by late autumn. Typical C3 cold season turfgrasses with optimal temperatures in the 15~25°C range include blue grass and bentgrass varieties. The latter is particularly advantageous for the putting greens [1, 4, 5, 12]. In this chapter, the review will be concerned with two main varieties, zoysiagrass (
3. Transgenes and mechanisms of herbicidal action
Turfgrass has been a subject of classical breeding for trait improvement over decades, especially in Japan and United States. However, conventional breeding suffers from such drawbacks as low efficiency, time consuming and labor intensiveness. With an increasing trend in turfgrass cultivation worldwide, excessive applications of herbicides and other agrochemicals over the grass habitats adversely impact the environment, biodiversity and human health [13, 14]. Several attempts to develop GM turfgrass lines with improved traits have been reported; for example, herbicide-resistant turfgrass varieties in references [15], [16], 17] and [10] and insect-resistant turfgrass in reference [18]. A number of laboratories are developing herbicide-resistant and other transgenic turfgrasses with biotic and abiotic stress tolerances (Table 1).
So far, several genes including the two widely adopted ones,
The widely used herbicide, bialaphos (also phosphinothricin-alanyl-alanine tripeptide, PTT), is an antibiotic produced by certain
The glufosinate herbicide causes accumulation of lethal levels of ammonia in both soil bacteria and plant cells. The GS inhibiting activity of glufosinate is lost when its amino group is acetylated by a phosphinothricin acetyl transferase (PAT encoded by
Thus, a transgenic turfgrass transformed with
Glyphosate is a non-selective herbicidal agent commercialized under the trade name “Roundup” by Monsanto. It exerts its herbicidal action by competitively inhibiting the 5-enolpyruvylshikimate-3-phosphate synthase (EPSPs) centrally involved in the biosynthesis of aromatic amino acids (phenylalanine, tryptophan and tyrosine). Plants treated with glyphosate are killed for the lack of these amino acids in protein biosynthesis. Accumulation of shikimate also leads to cell death, thus contributing to the herbicidal action of glyphosate [20] (Figure. 3).
A transgenic bentgrass carrying the EPSPS gene (“Roundup Ready”) then develops resistance to Roundup [7, 21].
Although both
One of the most promising herbicide-resistant traits can be conferred by dicamba monooxygenase gene (
4. Herbicide-resistant zoysiagrass and bentgrass
In a previous report, we discussed the development of the
When zoysiagrass and possibly other turfgrass species are left unmanaged under natural habitats, their populations and swarth growth are easily overtaken by the dominant weed plants. Figure 6 shows our own observations of herbicide-resistant zoysiagrass plants growing in natural habitats during the four consecutive years (2006~2009). In four years, the ground coverage of zoysiagrass was dominated by the weeds when the grass plot was left unmanaged. On the other hand, the herbicide-resistant plants continued healthy population and swarth growths under managed conditions involving fertilizer applications, herbicide sprays and timely mowings.
Recently, we reported the development and morphological characterization of transgenic
We observed a delay in necrosis (senescence) of
5. Environmental risk assessment
To commercialize any of the transgenic turfgrass varieties listed in Table 1, their environmental risks must be assessed under their natural habitats [7, 8, 9, 25]. This chapter briefly reviews our own studies and discusses attempts to block or minimize the risks of gene flow from the transgenic turfgrass habitats to the plants at neighboring and remote sites. For example, in reference [26] and [27] the workers introduced a male-sterility gene into GM crops to block the escape of a transgene from the latter, and this strategy may be applied to turfgrasses. We developed a sterile herbicide-resistant zoysiagrass through γ-radiation mutation, making the latter unbolting and deficient in fertile pollens [28, 29]. The γ-radiation generated herbicide-resistant zoysiagrass can be cultivated in agronomic habitats for eventual commercialization [25].
A preliminary study showed that the transgene (
According to the “Weed risk assessments for Hawaii and Pacific Islands” database (http://www.botany.hawaii.edu/faculty/daehler/wra/default.htm), transgenic
Although the risk of transgene escape and flow from the genetically modified zoysiagrass is low, pollen-induced gene flow cannot be completely discounted. In reference [30] we examined the pollen releases from the defined boundary of
Figure 9 shows the sites in Jeju Island monitored for the potential gene flow from the herbicide-resistant
6. Commercial potentials and outlook
Turfgrass is a highly value-added crop in terms of commercial profits per land acreage, when compared to other crops. Turfgrasses sward vigorously through vegetative propagation and swarth growth. According to TPI data (Turfgrass Producers International), the turfgrass market size increased by 35% during the five year (2002-2007) period [31]. Based on the data available, transgenic zoysiagrasses pose considerably less risk of transgene escape than does bentgrass. Furthermore, the former can be effectively propagated vegetatively, and sterile herbicide-resistant zoysiagrass (and bentgrass) can be developed through γ-radiation treatment [30]. This will circumvent to a large extent the public’s objections to genetically modified plants and their unintended escapes.
7. Conclusion
We compiled a table of transgenic herbicide-resistant turfgrass varieties in various stages of development and eventual agronomic cultivations. As can be seen in Table 1 of this chapter, several transgenes have been introduced into zoysiagrass, bentgrass and other lawn grass species primarily through Agrobacterium-mediated transformation and biolistic transfection. These grasses all exhibit resistance to their intended herbicides such as Basta, Roundup and others, but how well each of the transgenics developed performs in test plots and natural habitats cannot be assessed at this point largely because quantitative data such as the dose-response curves and the outdoor performances are lacking in most cases. In this chapter, we focused our discussion to the
Acknowledgments
This research was supported by Next-Generation Biogreen 21 Program, Rural Development Administration, Republic of Korea (Grant No. PJ00949901), Basic Science Research Program (NRF Grant No. 2012R1A1A2000706 to PSS, 2012-0004335) and the Priority Research Centers Program (2012048080) through the National Research Foundation of Korea (NRF) funded by the Ministry of Education, Science and Technology.References
- 1.
Kim K.N. Introductory turfgrass science. (in Korean) Sahmyook University; 2005. - 2.
Pessarakli M. Turfgrass Management and Physiology. USA: CRC Press; 2007. - 3.
Takebayashi H., Moriyama M. Study on the urban heat island mitigation effect achieved by converting to grass-covered parking. Solar Energy 2009; 83(8) 1211-1223. - 4.
Lee L. Turfgrass biotechnology. Plant Science 1996; 115(1) 1-8. - 5.
Spangenberg G., Wang Z.Y., Potrykus I. Biotechnology in Forage and Turf Grass Improvement. Berlin: Springer; 1998. - 6.
Zilinskas B.A., Wang X. Genetic transformation of turfgrass, In: Liang GH, Skinner DZ, (eds). Genetically Modified Crops: Their Development, Uses, and Risks. New York: Food Product Press; 2004. p309-350. - 7.
Watrud L.S., Lee E.H., Fairbrother A., Burdick C., Reichman J.R., Bollman M., Storm M., KIng G., Van de Water P.K. Evidence for landscape-level, pollen-mediated gene flow from genetically modified creeping bentgrass with CP4 EPSPS as a marker. Proceedings of the National Academy of Sciences 2004; 101(40) 14533-14538. - 8.
Reichman J.R., Watrud L.S., Lee E.H., Burdick C.A., Bollman M.A., Storm M.J., King G.A., Mallory-Smith C. Establishment of transgenic herbicide-resistant creeping bentgrass ( Agrostis stolonifera L.) in nonagronomic habitats. Molecular Ecology 2006; 15(13) 4243-4255. - 9.
Bae T.W., Vanjildorj E., Song S.Y., Nishiguchi S., Yang S.S., Song I.J., Chandrasekhar T., Kang T.W., Kim J.L., Koh Y.J., Park S.Y., Lee J., Lee Y.E., Ryu K.H., Riu K.Z., Song P.S., Lee H.Y. Environmental risk assessment of genetically engineered herbicide-tolerant Zoysia japonica . Journal of Environmental Quality 2008; 37(1) 207-218. - 10.
Ganesan M., Han Y.J., Bae T.W., Hwang O.J., Chandrasekkhar T., Shin A.Y., Goh C.H., Nishiguchi S., Song I.J., Lee H.Y., Kim J.I., Song P.S. Overexpression of phytochrome A and its hyperactive mutant improves shade tolerance and turf quality in creeping bentgrass and zoysiagrass. Planta 2012; 236(4) 1135-1150. - 11.
Guo S.X., Harriman R., Lee L., Nelson E.K. Bentgrass event ASR-368 and compositions and methods for detection thereof, United States Patent Number 7569747B2; 2009. - 12.
Fry J., Huang B. Applied Turfgrass Science and Physiology. Hoboken, NJ, USA: John Wiley & Sons; 2004. - 13.
Choi J.S., Fermanian T.W., Wehner D.J., Spomer L.A. Effect of temperature, moisture and soil texture on DCPA degradation. Agronomy Journal 1990; 80(1) 108-113. - 14.
Schleicher L.C., Shea P.J., Stougaard R.N., Tupy D.R. Efficacy and dissipation of dithiopyr and pendimethalin in perennial ryegrass ( Lolium perenne ) turf. Weed Science 1995; 43(1) 140-148. - 15.
Toyama K., Bae C.H., Kang J.G., Lim Y.P., Adachi T., Riu K.Z., Song P.S., Lee H.Y. Production of herbicide-tolerant zoysiagrass by Agrobacterium -mediated transformation. Molecules and Cells 2003; 16(1) 19-27. - 16.
Fu D., Tisserat N.A., Xiao Y., Settleb D., Muthukrishnan S., Liang G.H. Overexpression of rice TLPD34 enhances dollar-spot resistance in transgenic bentgrass. Plant Science 2005; 168(3) 671-680. - 17.
Ge Y, Norton T, Wang ZY. Transgenic Zoysiagrass ( Zoysia japonica ) plants obtained byAgrobacterium -mediated transformation. Plant Cell Reports 2006; 25(8) 792-798. - 18.
Zhang L., Wu D., Zhang L., Yang C. Agrobacterium mediated transformation of Japanese lawn grass (Zoysia japonica Steud.) containing a synthetic crylA(b) gene fromBacillus thuringiensis . Plant Breed. 2007; 126(4) 428-432. - 19.
Bayer E., Gugel K.H., Hägele K., Hagenmaier H., Jessipow S., König W.A., Zöhner H. Phosphinothricin and Phosphinothritcyl-Alanyl-Alanin. Helvetica Chimica Acta 1972: 55 224-239. - 20.
Weed Science Society of America. WSSA: Society, Press Room: Weed Control. http://www.wssa.net/WSSA/PressRoom/index.htm (accessed 19 Dec 2007). - 21.
Nelson E., Stone T. Petition for determination of non-regulated status: Roundup Ready Creeping Bent grass Event ASF368. Petition #01-TR-054U [www.aphis.usda.gov/brs/not_reg.html] 2003. - 22.
Lee K.W., Kim K.Y., Kim K.H., Lee B.H., Kim J.S., Lee S.H. Development of antibiotic marker-free creeping bentgrass resistance against herbicides. Acta Biochim Biophys Sin 2011; 43(1) 13-18. - 23.
Behrens M.R., Mutlu N., Chakraborty S., Dumitru R., Jiang W.Z., LaVallee B.J., Herman P.L., Clemente T.E., Weeks D.P. Dicamba resistance: enlarging and preserving biotechnology-based weed management strategies. Science 2007; 316(5828) 1185-1188. - 24.
Kim J.I., Shen Y., Han Y.J., Park J.E., Kirchenbauer D., Soh M.S., Nagy F., Schäfer E., Song P.S. Phytochrome phosphorylation modulates light signaling by influencing the protein-protein interaction. The Plant Cell 2004; 16(10) 2629-2640. - 25.
Bae T.W., Kang H.G., Song I.J., Sun H.J., Ko S.M., Song P.S., Lee H.Y. Environmental risk assessment of genetically modified herbicide-tolerant zoysiagrass (Event: Jeju Green21). (in Korean) Journal of Plant Biotechnology 2011; 38(2) 105-116. - 26.
Khan M.S. Plant biology: engineered male sterility. Nature 2005; 436: 783-785. - 27.
Ruiz O.N., Daniell H. Engineering cytoplasmic male sterility via the chloroplast genome by expression of beta-ketothiolase. Plant Physiology 2005; 138(3) 1232-1246. - 28.
Bae T.W., Kim J., Song I.J., Song S.Y., Lim P.O., Song P.S., Lee H.Y. Production of unbolting lines through gamma-ray irradiation mutagenesis in genetically modified herbicide-tolerant Zoysia japonica . Breeding Science 2009; 59(1) 103-105. - 29.
Bae T.W., Song I.J., Kang H.G., Jeong O.C., Sun H.J., Ko S.M., Lim P.O., Song P.S., Song S.J., Lee H.Y. Selection of male-sterile and dwarfism genetically modified Zoysia japonica through gamma irradiation. (in Korean) Journal of Radiation Industry 2010; 4(3) 239-246. - 30.
Kang H.G., Bae T.W., Jeong O.C., Sun H.J., Lim P.O., Lee H.Y. Evaluation of viability, shedding pattern, and longevity of pollen from genetically, modified (GM) herbicide- tolerant and wild-type zoysiagrass ( Zoysia japonica Steud.). Journal of Plant Biology 2009; 52(6) 630-634. - 31.
Turfgrass Producers International. TPI: Professional Resources, TPI products, Surveys: 2007 USDA AG Census report. http://www.turfgrasssod.org/pages/resources/usda-ag census-reports (accessed April 2009). - 32.
Priestman M.A., Funke T., Singh I.M., Crupper S.S., Schönbrunn E. 5-enolpyruvylshikimate 3-phosphate synthase from Staphylococcus aureus is insensitive to glyphosate. Federation of European Biochemical Societies 2005; 579(3) 728-732. - 33.
Fu D., Huang B., Xiao Y, Muthukrishnan S, Liang G.H. Overexpression of barley hva1 gene in creeping bentgrass for improving drought tolerance. Plant Cell Reports 2007; 26 467-477. - 34.
Cho K.C., Han Y.J., Kim S.J., Lee S.S., Hwang O.J., Song P.S., Kim Y.S., Kim J.I. Resistance to Rhizoctonia solani AG-2-2 (IIIB) in creeping bentgrass plants transformed with pepper esterase genePepEST . Plant Pathology 2011; 60(4) 631-639. - 35.
Han Y.J., Kim Y.M., Lee J.Y, Kim S.J., Cho K.C., Chandrasekhar T., Song P.S., Woo Y.M., Kim J.I. Production of purple-colored creeping bentgrass using maize transcription factor genes Pl andLc throughAgrobacterium -mediated transformation. Plant Cell Reports 2009; 28(3) 397-406. - 36.
Han Y.J., Cho K.C., Hwang O.J., Choi Y.S., Shin A.Y., Hwang I., Kim J.I. Overexpression of an Arabidopsis b-glucosidase gene enhances drought resistance with dwarf phenotype in creeping bentgrass. Plant Cell Reports 2012; 31(9) 1677-1686. - 37.
Kim S.J., Lee J.Y., Kim Y.M., Yang S.S., Hwang O.J., Hong N.J., Kim K.M., Lee H.Y., Song P..S, Kim J.I. Agrobacterium -mediated high-efficiency transformation of creeping bentgrass with herbicide resistance. Journal of Plant Biology 2007; 50(5) 577-585. - 38.
Asano Y., Ito Y., Fukami M., Morifuji A. Production of herbicide resistant transgenic creeping bent plants. International Turfgrass Society Research Journal 2007; 8 261-267. - 39.
Asano Y., Ito Y., Fukami M., Sugiura K., Fujiie A. Herbicide-resistant transgenic creeping bentgrass plants obtained by electroporation using an altered buffer. Plant Cell Reports 1998; 17(12) 963-967. - 40.
Aswath C.R., Kim S.H., Mo S.Y., Kim D.W. Transgenic plants of creeping bent grass harboring the stress inducible gene, 9-cis-epoxycarotenoid dioxygenase, are highly tolerant to drought and NaCl stress. Plant Growth Regulation 2005; 47(2/3) 129-139. - 41.
Yang D.H, Sun H.J., Goh C.H., Song P.S., Bae T.W., Song I.J., Lim Y.P., Lim P.O., Lee H.Y. Cloning of a Zoysia ZjLsL and its overexpression to induce axillary meristem initiation and tiller formation inArabidopsis and bentgrass. Plant Biology 2012; 14(3) 411-419. - 42.
Wang Y., Kausch A.P., Chandlee J.M., Luo H., Ruemmele B.A., Browning M., Jackson N., Goldsmith M.R. Co-transfer and expression of chitinase, glucanase, and bar genes in creeping bentgrass for conferring fungal disease resistance. Plant Science 2003; 165(3) 497-506. - 43.
Luo H., Hu Q., Nelson K., Longo C., Kausch A.P., Chandlee J.M., Wipff J.K., Fricker C.R. Agrobacterium tumefaciens-mediated creeping bentgrass (Agrostis stolonifera L.) transformation using phosphinothricin selection results in a high frequency of single-copy transgene integration. Plant Cell Reports 2004; 22(9) 645-652. - 44.
Zhou M., Hu Q., Li Z., Li D., Chen C.F., Luo H. Expression of a novel antimicrobial peptide Penaeidin4-1 in creeping bentgrass ( Agrostis stolonifera L.) enhances plant fungal disease resistance. PLoS One 2011; 6(9) 1-12. - 45.
Li Z., Baldwin C.M., Hu Q., Liu H., Luo H. Heterologous expression of Arabidopsis H+-pyrophosphatase enhances salt tolerance in transgenic creeping bentgrass (Agrostis stolonifera L.). Plant, Cell & Environment 2010; 33(2) 272-289. - 46.
Hartman C.L., Lee L., Day P.R., Tumer N.E. Herbicide Resistant Turfgrass ( Agrostis palustris Huds.) by Biolistic Transformation. Nature Biotechnology 1994; 12 919-923. - 47.
Chai M.L., Wang B.L., Kim J.Y., Lee J.M., Kim D.H. Agrobacterium -mediated transformation of herbicide resistance in creeping bentgrass and colonial bentgrass. Journal of Zhejiang University Science 2003; 4(3) 346-351 - 48.
Lee L., Laramore C.L., Day P.R., Tumer N.E. Transformation and regeneration of creeping bentgrass ( Agrostis palustris Huds.) protoplasts. Crop Science 1996; 36(2) 401-406. - 49.
Chai B., Maqbool S.B., Hajela R.K., Green D., Vargas Jr J.M., Warkentin D., Sabzikar R., Sticklen M.B. Cloning of a chitinase-like cDNA ( hs2 ), its transfer to creeping bentgrass (Agrostis palustris Huds.) and development of brown patch (Rhizoctonia solani ) disease resistant transgenic lines. Plant Science 2002; 163(2) 183-193. - 50.
Goldman J.J., Hanna W.W., Fleming G.H., Ozias-Akins P. Ploidy variation among herbicide-resistant bermudagrass plants of cv. TifEagle transformed with the bar gene. Plant Cell Reports 2004; 22(8) 553-560. - 51.
Hu F., Zhang L., Wang X., Ding J., Wu D.. Agrobacterium -mediated transformed transgenic triploid bermudagrass (Cynodon dactylon XC. transvaalensis ) plants are highly resistant to the glufosinate herbicide Liberty. Plant Cell, Tissue and Organ Culture 2005; 83(1) 13-19. - 52.
Denchev P.D., Songstad D.D., McDaniel J.K., Conger B.V. Transgenic orchardgrass ( Dactylis glomerata ) plants by direct embryogenesis from microprojectile bombarded leaf cells. Plant Cell Reports 1997; 16(12) 813-819. - 53.
Cho M.J., Choi H.W., Lemaux P.G. Transformed T0 orchardgrass ( Dactylis glomerata L.) plants produced from highly regenerative tissues derived from mature seeds. Plant Cell Reports 2001; 20(4) 318-324. - 54.
Wang Z.Y., Takamizo T., Iglesias V.A., Osusky M., Nagel J., Potrykus I., Spangenberg G. Transgenic plants of tall fescue ( Festuca arundinacea Schreb.) obtained by direct gene transfer to protoplasts. Biotechnology 1992; 10(6) 691-696. - 55.
Hu Y., Jia W., Wang J., Zhang Y., Yang L., Lin Z. Transgenic tall fescue containing the Agrobacterium tumefaciens ipt gene shows enhanced cold tolerance. Plant Cell Reports 2005; 23(10-11) 705-709. - 56.
Spangenberg G., Wang Z.Y., Nagel J., Potrykus I. Protoplast culture and generation of transgenic plants in red fescue ( Festuca rubra L.). Plant Science 1994; 97(1) 83-94. - 57.
Hisano H., Kanazawa A., Kawakami A., Yoshida M., Shimamoto Y., Yamada T. Transgenic perennial ryegrass plants expressing wheat fructosyltransferase genes accumulate increased amounts of fructan and acquire increased tolerance on a cellular level to freezing. Plant Science 204; 167(4) 861-868. - 58.
Wu Y.Y., Chen Q.J., Chen M., Chen J., Wang X.C. Salt-tolerant transgenic perennial ryegrass ( Lolium perenne L.) obtained byAgrobacterium tumefaciens -mediated transformation of the vacuolar Na+/H+ antiporter gene. Plant Science 2005; 169(1) 65-73. - 59.
Richards H.A., Rudas V.A., Sun H., McDaiel J.K., Tomaszewski Z., Conger B.V. Construction of a GFP-BAR plasmid and its use for switchgrass transformation. Plant Cell Reports 2001; 20(1) 48-54. - 60.
Somleva M.N., Tomaszewski Z., Conger B.V. Agrobacterium -mediated genetic transformation of switchgrass. Crop Science 2002; 42(6) 2080-2087. - 61.
Smith R.L., Grando M.F., Li Y.Y., Seib J.C., Shatters R.G. Transformation of bahiagrass ( Paspalum notatum Flugge). Plant Cell Reports. 2002; 20(11) 1017-1021. - 62.
Gondo T., Tsurta S.I., Akashi R., Kawamura O., Hoffmann F. Green, herbicide-resistant plants by particle inflow gun-mediated gene transfer to diploid bahiagrass ( Paspalum notatum ). Journal of Plant Physiology 2005; 162(12) 1367-1375. - 63.
Kim K.M., Song I.J., Lee H.Y., Raymer P., Kim B.S., Kim W. Development of seashore paspalum turfgrass with herbicide resistance. 2009; Korean Journal of crop science 54(4) 427-432. - 64.
Lim S.H., Kang B.C., Shin H.K.. Herbicide Resistant Turfgrass ( Zoysia japonica cv. 'Zenith') Plants by Particle bombardment-mediated Transformation. 2004; Korean journal of turfgrass science 18(4) 211 – 219. - 65.
Li R.F., Wei J.H., Wang H.Z., He J., Sun Z.Y. Development of highly regenerable callus lines and -mediated transformation of Chinese lawngrass (Agrobacterium Zoysia sinica Hance) with a cold inducible transcription factor, CBF1. Plant Cell, Tissue and Organ Culture 2006; 85(3): 297-305.