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Plant function and evolutionary biology
RESEARCH ARTICLE

Impact of defoliation severity on photosynthesis, carbon metabolism and transport gene expression in perennial ryegrass

Julia M. Lee A D , Puthigae Sathish B , Daniel J. Donaghy C and John R. Roche A
+ Author Affiliations
- Author Affiliations

A DairyNZ Ltd, Private Bag 3221, Hamilton 3240, New Zealand.

B Pastoral Genomics, ViaLactia Biosciences (NZ) Ltd, PO Box 109185, Newmarket, Auckland 1149, New Zealand.

C University of Tasmania, PO Box 3523, Burnie, Tas. 7320, Australia.

D Corresponding author. Email: julia.lee@dairynz.co.nz

Functional Plant Biology 38(10) 808-817 https://doi.org/10.1071/FP11048
Submitted: 15 February 2011  Accepted: 9 June 2011   Published: 16 September 2011

Abstract

Defoliation severity affects grass regrowth. The changes to biological processes affecting regrowth induced by severe defoliation are not fully understood, nor have they been investigated at a molecular level in field-grown plants. Field-grown perennial ryegrass (Lolium perenne L.) plants were defoliated to 20, 40 or 60 mm during winter. Throughout regrowth, transcript profiles of 17 genes involved in photosynthesis and carbon metabolism or transport were characterised in stubble and lamina tissue. Although defoliation to 20 mm reduced residual lamina area and stubble water-soluble carbohydrate reserves compared with plants defoliated to 40 or 60 mm, net herbage regrowth was not reduced. Transcript profiles indicated a potential compensatory mechanism that may have facilitated regrowth. At the one-leaf regrowth stage, plants defoliated to 20 mm had greater abundance of photosynthesis-related gene transcripts (rca, rbcS1, rbcS2, fba, fbp and fnr) and 20% greater stubble total nitrogen than plants defoliated to 60 mm. A greater capacity for photosynthesis in outer leaf sheaths may be one potential mechanism used by severely defoliated plants to compensate for the reduced residual lamina area; however, this premise requires further investigation.

Additional keywords: defoliation intensity, nitrogen, pasture, regrowth, water-soluble carbohydrates.


References

Alba R, Fei Z, Payton P, Liu Y, Moore SL, Debbie P, Cohn J, D’Ascenzo M, Gordon JS, Rose JKC, Martin G, Tanksley SD, Bouzayen M, Jahn MM, Giovannoni J (2004) ESTs, cDNA microarrays, and gene expression profiling: tools for dissecting plant physiology and development. The Plant Journal 39, 697–714.
ESTs, cDNA microarrays, and gene expression profiling: tools for dissecting plant physiology and development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXos1ylt7w%3D&md5=173c588d2272832606227e5c757939e4CAS |

Andersen CL, Jensen JL, Orntoft TF (2004) Normalization of real-time quantitative reverse transcription-PCR data: a model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Research 64, 5245–5250.
Normalization of real-time quantitative reverse transcription-PCR data: a model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmtF2mtbg%3D&md5=1c92f9e60d0b91d5c373ffbfded10533CAS |

Barone A, Di Matteo A, Carputo D, Frusciante L (2009) High-throughput genomics enhances tomato breeding efficiency. Current Genomics 10, 1–9.
High-throughput genomics enhances tomato breeding efficiency.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXks1Chu7c%3D&md5=a22a6b5dec7be39d731fa8fd3bb4fdbeCAS |

Berthier A, Desclos M, Amiard V, Morvan-Bertrand A, Demmig-Adams B, Adams WW, Turgeon R, Prud’homme MP, Noiraud-Romy N (2009) Activation of sucrose transport in defoliated Lolium perenne L.: an example of apoplastic phloem loading plasticity. Plant & Cell Physiology 50, 1329–1344.
Activation of sucrose transport in defoliated Lolium perenne L.: an example of apoplastic phloem loading plasticity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXovVCitLo%3D&md5=27a555361249936b69e0e29f46c16f29CAS |

Bläsing OE, Gibon Y, Bläsing OE, Gibon Y, Gunther M, Hohne M, Morcuende R, Osuna D, Thimm O, Usadel B, Scheible WR, Stitt M (2005) Sugars and circadian regulation make major contributions to the global regulation of diurnal gene expression in Arabidopsis. The Plant Cell 17, 3257–3281.
Sugars and circadian regulation make major contributions to the global regulation of diurnal gene expression in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |

Booysen PV, Nelson CJ (1975) Leaf area and carbohydrate reserves in regrowth of tall fescue. Crop Science 15, 262–266.
Leaf area and carbohydrate reserves in regrowth of tall fescue.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2MXksVShsbc%3D&md5=8753ddba0ccf0826b64ab30c7e99a526CAS |

Borland AM, Farrar JF (1985) Diel patterns of carbohydrate metabolism in leaf blades and leaf sheaths of Poa annua L. and Poa × Jemtlandica (Almq.) Richt. New Phytologist 100, 519–531.
Diel patterns of carbohydrate metabolism in leaf blades and leaf sheaths of Poa annua L. and Poa × Jemtlandica (Almq.) Richt.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXltlylur8%3D&md5=6ab0077193dba2fc0650fbe0073f9c81CAS |

Brougham RW (1956) Effect of intensity of defoliation on regrowth of pasture. Australian Journal of Agricultural Research 7, 377–387.
Effect of intensity of defoliation on regrowth of pasture.Crossref | GoogleScholarGoogle Scholar |

Brougham RW (1957) Pasture growth rate studies in relation to grazing management. Proceedings of the New Zealand Society of Animal Production 17, 46–55.

Chalmers J, Lidgett A, Cummings N, Cao Y, Forster J, Spangenberg G (2005) Molecular genetics of fructan metabolism in perennial ryegrass. Plant Biotechnology Journal 3, 459–474.
Molecular genetics of fructan metabolism in perennial ryegrass.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVKltbvP&md5=12a21873865f0bea193fe607cdd4e860CAS |

Cho YH, Sheen J, Yoo SD (2010) Low glucose uncouples hexokinase1-dependent sugar signaling from stress and defense hormone abscisic acid and C2H4 responses in Arabidopsis. Plant Physiology 152, 1180–1182.
Low glucose uncouples hexokinase1-dependent sugar signaling from stress and defense hormone abscisic acid and C2H4 responses in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXmsF2ls7o%3D&md5=e71c349211641562d486c176d613289dCAS |

Davies A (1965) Carbohydrate levels and regrowth in perennial ryegrass. The Journal of Agricultural Science 65, 213–221.
Carbohydrate levels and regrowth in perennial ryegrass.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF28XhtlSjsQ%3D%3D&md5=6c746ef1252e1a888bbbc854193ef34fCAS |

Evans JR (1989) Photosynthesis and nitrogen relationships in leaves of C3 plants. Oecologia 78, 9–19.
Photosynthesis and nitrogen relationships in leaves of C3 plants.Crossref | GoogleScholarGoogle Scholar |

Flores HE, Dai Y, Cuello JL, Maldonado-Mendoza IE, Loyola-Vargas VM (1993) Green roots: photosynthesis and photoautotrophy in an underground plant organ. Plant Physiology 101, 363–371.

Fulkerson WJ, Donaghy DJ (2001) Plant-soluble carbohydrate reserves and senescence – key criteria for developing an effective grazing management system for ryegrass-based pastures: a review. Australian Journal of Experimental Agriculture 41, 261–275.
Plant-soluble carbohydrate reserves and senescence – key criteria for developing an effective grazing management system for ryegrass-based pastures: a review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjslKltbo%3D&md5=6dac2ab67da5cb993e0aea1fea3beffbCAS |

Fulkerson WJ, Michell PJ (1987) The effect of height and frequency of mowing on the yield and composition of perennial ryegrass–white clover swards in the autumn to spring period. Grass and Forage Science 42, 169–174.
The effect of height and frequency of mowing on the yield and composition of perennial ryegrass–white clover swards in the autumn to spring period.Crossref | GoogleScholarGoogle Scholar |

Fulkerson WJ, Slack K (1995) Leaf number as a criterion for determining defoliation time for Lolium perenne: 2. Effect of defoliation frequency and height. Grass and Forage Science 50, 16–20.
Leaf number as a criterion for determining defoliation time for Lolium perenne: 2. Effect of defoliation frequency and height.Crossref | GoogleScholarGoogle Scholar |

Fulkerson WJ, Slack K, Lowe KF (1994) Variation in the response of Lolium genotypes to defoliation. Australian Journal of Agricultural Research 45, 1309–1317.
Variation in the response of Lolium genotypes to defoliation.Crossref | GoogleScholarGoogle Scholar |

Graham IA, Martin T (2000) Control of photosynthesis, allocation and partitioning by sugar related gene expression. In ‘Photosynthesis: physiology and metabolism. Vol. 9’. (Eds RC Leegood, TD Sharkey, S von Caemmerer) pp. 233–248. (Kluwer Academic Publishers: Dordrecht)

Harrison MT, Kelman WM, Moore AD, Evans JR (2010) Grazing winter wheat relieves plant water stress and transiently enhances photosynthesis. Functional Plant Biology 37, 726–736.
Grazing winter wheat relieves plant water stress and transiently enhances photosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXpt1Ckt7Y%3D&md5=37ab81e016ba83162d1c58ab5b05b020CAS |

Hisano H, Kanazawa A, Yoshida M, Humphreys MO, Iizuka M, Kitamura K, Yamada T (2008) Coordinated expression of functionally diverse fructosyltransferase genes is associated with fructan accumulation in response to low temperature in perennial ryegrass. New Phytologist 178, 766–780.
Coordinated expression of functionally diverse fructosyltransferase genes is associated with fructan accumulation in response to low temperature in perennial ryegrass.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXnsFKqtbg%3D&md5=3d8e287c4fc4a695bddd6583d62d3aeeCAS |

Khaembah EA (2009) Leaf Rubisco turnover variation in a perennial ryegrass (Lolium perenne L.) population: analysis of quantitative trait loci, implications for productivity, and potential for manipulation. PhD Thesis, Massey University, Palmerston North, New Zealand.

Koch KE (1996) Carbohydrate-modulated gene expression in plants. Annual Review of Plant Physiology and Plant Molecular Biology 47, 509–540.
Carbohydrate-modulated gene expression in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XjtlWgtrY%3D&md5=289c4c5de4a1fcfb1e95a677b5331623CAS |

Krapp A, Hofmann B, Schäfer C, Stitt M (1993) Regulation of the expression of rbcS and other photosynthetic genes by carbohydrates: a mechanism for the ‘sink regulation’ of photosynthesis? The Plant Journal 3, 817–828.
Regulation of the expression of rbcS and other photosynthetic genes by carbohydrates: a mechanism for the ‘sink regulation’ of photosynthesis?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXmt1Wqtb4%3D&md5=8a5b38de38ec1d056fce7ce723cb3543CAS |

Lee JM, Donaghy DJ, Roche JR (2008) Effect of defoliation severity on regrowth and nutritive value of perennial ryegrass (Lolium perenne L.) dominant swards. Agronomy Journal 100, 308–314.
Effect of defoliation severity on regrowth and nutritive value of perennial ryegrass (Lolium perenne L.) dominant swards.Crossref | GoogleScholarGoogle Scholar |

Lee JM, Donaghy DJ, Sathish P, Roche JR (2009) Interaction between water-soluble carbohydrate reserves and defoliation severity on the regrowth of perennial ryegrass (Lolium perenne L.)-dominant swards. Grass and Forage Science 64, 266–275.
Interaction between water-soluble carbohydrate reserves and defoliation severity on the regrowth of perennial ryegrass (Lolium perenne L.)-dominant swards.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFGhsbbN&md5=1250b106cbfb286c928e8f5c70f1c00dCAS |

Lee JM, Roche JR, Donaghy DJ, Thrush A, Sathish P (2010a) Validation of reference genes for quantitative RT-PCR studies of gene expression in perennial ryegrass (Lolium perenne L.). BMC Molecular Biology 11, 8
Validation of reference genes for quantitative RT-PCR studies of gene expression in perennial ryegrass (Lolium perenne L.).Crossref | GoogleScholarGoogle Scholar |

Lee JM, Sathish P, Donaghy DJ, Roche JR (2010b) Plants modify biological processes to ensure survival following carbon depletion: a Lolium perenne model. PLoS ONE 5, e12306
Plants modify biological processes to ensure survival following carbon depletion: a Lolium perenne model.Crossref | GoogleScholarGoogle Scholar |

Long SP, Ainsworth EA, Leakey ADB, Nosberger J, Ort DR (2006) Food for thought: lower-than-expected crop yield stimulation with rising CO2 concentrations. Science 312, 1918–1921.
Food for thought: lower-than-expected crop yield stimulation with rising CO2 concentrations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XmsVagsr4%3D&md5=8a97c04e71bbb18e8c2a7ff1f07b569fCAS |

Lytovchenko A, Sonnewald U, Fernie AR (2007) The complex network of non-cellulosic carbohydrate metabolism. Current Opinion in Plant Biology 10, 227–235.
The complex network of non-cellulosic carbohydrate metabolism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXlt1Sitrg%3D&md5=5f9df81d948d6387de127d31f4d0f254CAS |

McCormick AJ, Cramer MD, Watt DA (2008) Changes in photosynthetic rates and gene expression of leaves during a source sink perturbation in sugarcane. Annals of Botany 101, 89–102.
Changes in photosynthetic rates and gene expression of leaves during a source sink perturbation in sugarcane.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXitlans7s%3D&md5=005ed86fb8ded1686817d5d773a81986CAS |

McKenzie F, Jacobs J, Ward G (2004) Dairy pasture yield and growth responses to summer and spring grazing. In ‘Proceedings of the Thirty-fourth Annual Conference, Agronomy Society of New Zealand, Ashburton, New Zealand’. pp. 21–30.

Morvan-Bertrand A, Boucaud J, Prud’homme MP (1999) Influence of initial levels of carbohydrates, fructans, nitrogen and soluble proteins on regrowth of Lolium perenne L. cv. Bravo following defoliation. Journal of Experimental Botany 50, 1817–1826.
Influence of initial levels of carbohydrates, fructans, nitrogen and soluble proteins on regrowth of Lolium perenne L. cv. Bravo following defoliation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXntFOnug%3D%3D&md5=aee7bc5d0b060ffe09a385116f553893CAS |

Morvan-Bertrand A, Boucaud J, Le Saos J, Prud’homme MP (2001) Roles of the fructans from leaf sheaths and from the elongating leaf bases in the regrowth following defoliation of Lolium perenne L. Planta 213, 109–120.
Roles of the fructans from leaf sheaths and from the elongating leaf bases in the regrowth following defoliation of Lolium perenne L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjt1ChsL0%3D&md5=1701425fd8a5892be8e4863c2f5f4e99CAS |

Nowak RS, Caldwell MM (1984) A test of compensatory photosynthesis in the field: implications for herbivory tolerance. Oecologia 61, 311–318.
A test of compensatory photosynthesis in the field: implications for herbivory tolerance.Crossref | GoogleScholarGoogle Scholar |

Öpik H, Rolfe SA, Willis AJ, Street HE (2005) ‘The physiology of flowering plants.’ (Cambridge University Press: Cambridge, UK)

Parsons AJ, Chapman DF (2000) The principles of pasture growth and utilization. In ‘Grass: its production and utilization’. (Ed. A Hopkins) pp. 31–89. (Blackwell Science Ltd: Oxford)

Paul MJ, Pellny TK (2003) Carbon metabolite feedback regulation of leaf photosynthesis and development. Journal of Experimental Botany 54, 539–547.
Carbon metabolite feedback regulation of leaf photosynthesis and development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhsFKgtbY%3D&md5=bbc7e25043bd8daff087f9ccf9749f88CAS |

Portis A (2003) Rubisco activase – Rubisco’s catalytic chaperone. Photosynthesis Research 75, 11–27.
Rubisco activase – Rubisco’s catalytic chaperone.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXht1Krurk%3D&md5=8b3c66599938ce452e70e2cccd10a533CAS |

Rasmussen S, Parsons AJ, Rasmussen S, Parsons AJ, Bassett S, Christensen MJ, Hume DE, Johnson LJ, Johnson RD, Simpson WR, Stacke C, Voisey CR, Xue H, Newman JA (2007) High nitrogen supply and carbohydrate content reduce fungal endophyte and alkaloid concentration in Lolium perenne. New Phytologist 173, 787–797.
High nitrogen supply and carbohydrate content reduce fungal endophyte and alkaloid concentration in Lolium perenne.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjvFGgsbg%3D&md5=47ad2578d7ccbef3d15748d5036b268fCAS |

Reid D (1959) Studies on the cutting management of grass–clover swards. 1. The effect of varying the closeness of cutting on the yields from an established grass-clover sward. The Journal of Agricultural Science 53, 299–312.
Studies on the cutting management of grass–clover swards. 1. The effect of varying the closeness of cutting on the yields from an established grass-clover sward.Crossref | GoogleScholarGoogle Scholar |

Rensink WA, Buell CR (2004) Arabidopsis to rice. Applying knowledge from a weed to enhance our understanding of a crop species. Plant Physiology 135, 622–629.
Arabidopsis to rice. Applying knowledge from a weed to enhance our understanding of a crop species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXltlKjtbw%3D&md5=812941fce23af19bf5134bc5b84cda8dCAS |

Rolland F, Baena-Gonzalez E, Sheen J (2006) Sugar sensing and signaling in plants: conserved and novel mechanisms. Annual Review of Plant Biology 57, 675–709.
Sugar sensing and signaling in plants: conserved and novel mechanisms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XosVKht7k%3D&md5=4a989c1b1f23e4c5e3a6200a6f7dcd7bCAS |

Rozen S, Skaletsky HJ (2000) Primer3 on the WWW for general users and for biologist programmers. In ‘Methods in molecular biology: bioinformatics methods and protocols. Vol. 132’. (Eds S Misener and SA Krawetz) pp. 365–386. (Humana Press: Totowa, NJ)

Sathish P, Withana N, Sathish P, Withana N, Biswas M, Bryant C, Templeton K, Al-Wahb M, Smith-Espinoza C, Roche JR, Elborough KM, Phillips JR (2007) Transcriptome analysis reveals season-specific rbcS gene expression profiles in diploid perennial ryegrass (Lolium perenne L.). Plant Biotechnology Journal 5, 146–161.
Transcriptome analysis reveals season-specific rbcS gene expression profiles in diploid perennial ryegrass (Lolium perenne L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXitV2juro%3D&md5=85520b8872258e084500282775c0a47fCAS |

Sawchuk MG, Donner TJ, Head P, Scarpella E (2008) Unique and overlapping expression patterns among members of photosynthesis-associated nuclear gene families in Arabidopsis. Plant Physiology 148, 1908–1924.
Unique and overlapping expression patterns among members of photosynthesis-associated nuclear gene families in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsFemtrnE&md5=9e6a7c0eab3bb8e620b5ccfa083920a6CAS |

Smith D (1969) Removing and analysing total non-structural carbohydrates from plant tissue. In ‘Research report no. 41’. pp. 1–11. (Wisconsin Agricultural Experimental Station: Madison)

Smith D (1974) Growth and development of timothy tillers as influenced by level of carbohydrate reserves and leaf area. Annals of Botany 38, 595–606.

Usami T, Mochizuki N, Kondo M, Nishimura M, Nagatani A (2004) Cryptochromes and phytochromes synergistically regulate Arabidopsis root greening under blue light. Plant & Cell Physiology 45, 1798–1808.
Cryptochromes and phytochromes synergistically regulate Arabidopsis root greening under blue light.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhsVCrt7k%3D&md5=b83d7b9529b63ec6dda98119dc627451CAS |

Varshney RK, Langridge P, Graner A (2007) Application of genomics to molecular breeding of wheat and barley. Advances in Genetics 58, 121–155.
Application of genomics to molecular breeding of wheat and barley.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtlOqu7Y%3D&md5=c0c6cbe7032f7f1f6c7cf9366af1689eCAS |

Verbyla AP, Cullis BR, Kenward MG, Welham SJ (1999) The analysis of designed experiments and longitudinal data by using smoothing splines (with discussion). Applied Statistics 48, 269–311.
The analysis of designed experiments and longitudinal data by using smoothing splines (with discussion).Crossref | GoogleScholarGoogle Scholar |

VSN International Ltd (2008) ‘Genstat Release 11 Reference Manual, Part 3 Procedure Library PL19.’ (VSN International Limited: Hemel Hempstead)

Wissel K, Pettersson F, Berglund A, Jansson S (2003) What affects mRNA levels in leaves of field-grown aspen? A study of developmental and environmental influences. Plant Physiology 133, 1190–1197.
What affects mRNA levels in leaves of field-grown aspen? A study of developmental and environmental influences.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXptFGitLw%3D&md5=e7e990c5072800faa512fb54d895f357CAS |