Research Interests

My research falls within the general area of plant responses to environmental stress. A particular focus is the study of crassulacean acid metabolism (CAM), a specialised mode of photosynthesis that results in substantial (i.e. up to 5 fold) improvement in plant water-use efficiency compared to other modes of photosynthesis (i.e. C3 and C4).  Examples of CAM plants include pineapple, prickly pear cactus, some orchids and Agave (used for production of Tequila!)

CAM is a relatively widespread adaptation to drought stress which has evolved in up to 7% of higher plants and permits the uptake of CO₂ at night. Since expression of the CAM pathway is readily modulated by the environment, CAM serves as a model system for establishing the functional significance of genes and enzymes that optimize physiological performance in arid, resource-limited habitats. Moreover, the day/night separation of carboxylation processes in the photosynthetic cells of CAM plants, poses fundamental questions in terms of metabolic control and circadian synchronization of metabolism.

The drivers of my research are to understand the metabolic basis of CAM in its various physiological manifestations and to use this information for exploiting the potential of naturally evolved and engineered CAM for sustainable productivity in a warmer and drier world. I am a project leader within a multi-institutional US Department of Energy (DOE) grant ($14 million) that seeks to engineer CAM into C3 crops as a means of enhancing plant water use efficiency (www.cambiodesign.org).

Current CAM projects at Newcastle include

• Metabolic determinants of CAM expression within the genus Clusia
  

Project leaders: Alastair Leverett, Anne Borland, Achim Treumann (Newcastle University Protein and Proteome Analysis)

• The role of primary metabolism in stomatal regulation in CAM plants 

Project leaders: Natalia Hurtado, Anne Borland, Tahar Taybi, James Hartwell (UL)

• The role of malate turnover in regulating physiological and biochemical aspects of CAM

Project leaders: Osita Nwokeocha, Anne Borland, Maxim Kapralov

• Molecular evolution of starch degradation in CAM guard cells

Project leaders: Danny Cowan-Turner, Anne Borland, Maxim Kapralov, James Hartwell (Liverpool), Achim Treumann (NUPPA)

Selected recent publications

Yang X, Hu R, Yin H  Borland AM, …. Cushman JC, Schmutz J, Tuskan GA (2017)The Kalanchoë genome provides insights into convergent evolution and building blocks of crassulacean acid metabolism. Nature Communications 8, 1899

Abraham PE, Yin H,  Borland, AM,  Weighill D,  Lim SD,  De Paoli HC, Engle N,  Jones PC,  Agh R, Weston DJ, Wullschleger SD, Tschaplinski T,  Jacobson D,  Cushman JC, Hettich RL, Tuskan GA, Yang X (2016) Transcript, protein and metabolite temporal dynamics in the CAM plant Agave. Nature Plants 2, 16178-16185.

Borland AM, Guo H-B, Yang X, Cushman JC (2016). Orchestration of carbohydrate processing for crassulacean acid metabolism. Current Opinion in Plant Biology 31: 118–124.

Borland AM, Hartwell J, Weston DJ, Tschaplinski TJ, Tuskan GA, Yang XH, Cushman JC. (2014) Engineering crassulacean acid metabolism to improve water-use efficiency. Trends in Plant Science 19, 327-338.

Borland AM, Wullschleger SD, Weston DJ, Hartwell J, Tuskan GA, Yang X, Cushman JC. (2014) Climate-resilient agroforestry: physiological responses to climate change and engineering of crassulacean acid metabolism (CAM) as a mitigation strategy. Plant Cell and Environment DOI 10.1111/pce.12479. 

De Pauli HC, Borland AM,  Tuskan GA, Cushman J, Yang X. (2014) Synthetic biology as it relates to CAM photosynthesis: challenges and opportunities. Journal of Experimental Botany 65, 3381-3393.

Barrera-Zambrano VA, Lawson TA, Olmos E, Fernandez-Garcia N, Borland AM. (2014) Leaf anatomical traits which accommodate the facultative engagement of CAM in tropical trees of the genus Clusia. Journal of Experimental Botany 65, 3513-3524. 

Ceusters J, Borland AM, Taybi T, Frans M, Godts C, De Proft MP. (2014) Light quality modulates metabolic synchronization over the diel phases of crassulacean acid metabolism. Journal of Experimental Botany 65, 3705-3714. 

Borland AM, Yang X (2013) Informing the improvement and biodesign of crassulacean acid metabolism via system dynamics modelling. New Phytologist 200, DOI:10.1111/nph.12529

Undergraduate Teaching

Stage 1:

Plant Biology 1 (BIO1003 Module leader)

Stage 3:

Plant Biology 3 (BIO3004 Module Leader)

Stage 3:  

Research projects (BIO3196) 

• Stabler D, Power E, Borland A, Barnes J, Wright G. A method for analysing small samples of floral pollen for free and protein-bound amino acids. Methods in Ecology and Evolution 2018, 9(2), 430-438.
• Power E, Stabler D, Borland AM, Barnes J, Wright GA. Analysis of nectar from low-volume flowers: a comparison of collection methods for free amino acids . Methods in Ecology and Evolution 2018, 9(3), 734–743.
• Liu D, Palla KJ, Hu R, Moseley RC, Mendoza C, Chen M, Abraham PE, Labbe JL, Kalluri UC, Tschaplinski TJ, Cushman JC, Borland AM, Tuskan GA, Yang X. Perspectives on the basic and applied aspects of crassulacean acid metabolism (CAM) research. Plant Science 2018, 274, 394-401.
• Taybi T, Cushman JC, Borland AM. Leaf carbohydrates influence transcriptional and post-transcriptional regulation of nocturnal carboxylation and starch degradation in the facultative CAM plant, Mesembryanthemum crystallinum. Journal of Plant Physiology 2017, 218, 144-154.
• Yang X, Hu R, Yin H, Jenkins J, Shu S, Tang H, Liu D, Weighill DA, Yim WC, Ha J, Heyduk K, Goodstein DM, Guo HB, Moseley RC, Fitzek E, Jawdy S, Zhang Z, Xie M, Hartwell J, Grimwood J, Abraham PE, Mewalal R, Beltran JD, Boxall SF, Dever LV, Palla KJ, Albion R, Garcia T, Mayer J, Lim SD, Wai CM, Peluso P, Buren RV, De Paoli HC, Borland AM, Guo H, Chen JG, Muchero W, Yin Y, Jacobson DA, Tschaplinski TJ, Hettich RL, Ming R, Winter K, Leebens-Mack JH, Smith JAC, Cushman JC, Schmutz J, Tuskan GA. The Kalanchoë genome provides insights into convergent evolution and building blocks of crassulacean acid metabolism. Nature Communications 2017, 8, 1899.
• Borland AM, Guo HB, Yang X, Cushman JC. Orchestration of carbohydrate processing for crassulacean acid metabolism. Current Opinion in Plant Biology 2016, 31, 118-124.
• Abraham PE, Yin H, Borland AM, Weighill D, Lim SD, DePaoli HC, Engle N, Jones PC, Agh R, Weston DJ, Wullschleger SD, Tschaplinski T, Jacobson D, Cushman JC, Hettich RL, Tuskan GA, Yang X. Transcript, protein, and metabolite temporal dynamics in the CAM plant Agave. Nature Plants 2016, 2, 16178.
• Yang XH, Cushman JC, Borland AM, Edwards EJ, Wullschleger SD, Tuskan GA, Owen NA, Griffiths H, Smith JAC, De Paoli HC, Weston DJ, Cottingham R, Hartwell J, Davis SC, Silvera K, Ming R, Schlauch K, Abraham P, Stewart JR, Guo HB, Albion R, Ha JM, Lim SD, Wone BWM, Yim WC, Garcia T, Mayer JA, Petereit J, Nair SS, Casey E, Hettich RL, Ceusters J, Ranjan P, Palla KJ, Yin HF, Reyes-Garcia C, Andrade JL, Freschi L, Beltran JD, Dever LV, Boxall SF, Waller J, Davies J, Bupphada P, Kadu N, Winter K, Sage RF, Aguilar CN, Schmutz J, Jenkins J, Holtum JAM. A roadmap for research on crassulacean acid metabolism (CAM) to enhance sustainable food and bioenergy production in a hotter, drier world. New Phytologist 2015, 207(3), 491-504.
• Borland AM, Wullschleger SD, Weston DJ, Hartwell J, Tuskan GA, Yang XH, Cushman JC. Climate-resilient agroforestry: physiological responses to climate change and engineering of crassulacean acid metabolism (CAM) as a mitigation strategy. Plant, Cell & Environment 2015, 38(9), 1833-1849.
• Cushman JC, Davis SC, Yang XH, Borland AM. Development and use of bioenergy feedstocks for semi-arid and arid lands. Journal of Experimental Botany 2015, 66(14), 4177-4193.
• Borland AM, Hartwell J, Weston DJ, Schlauch KA, Tschaplinski TJ, Tuskan GA, Yang XH, Cushman JC. Engineering crassulacean acid metabolism to improve water-use efficiency. Trends in Plant Science 2014, 19(5), 327-338.
• Zambrano VAB, Lawson T, Olmos E, Fernandez-Garcia N, Borland AM. Leaf anatomical traits which accommodate the facultative engagement of crassulacean acid metabolism in tropical trees of the genus Clusia. Journal of Experimental Botany 2014, 65(13), 3513-3523.
• Ceusters J, Borland AM, Taybi T, Frans M, Godts C, De Proft MP. Light quality modulates metabolic synchronization over the diel phases of crassulacean acid metabolism. Journal of Experimental Botany 2014, 65(13), 3705-3714.
• DePaoli HC, Borland AM, Tuskan GA, Cushman JC, Yang XH. Synthetic biology as it relates to CAM photosynthesis: challenges and opportunities. Journal of Experimental Botany 2014, 65(13), 3381-3393.
• Wright GA, Baker DD, Palmer MJ, Stabler D, Mustard JA, Power EF, Borland AM, Stevenson PC. Caffeine in Floral Nectar Enhances a Pollinator's Memory of Reward. Science 2013, 339(6124), 1202-1204.
• Borland AM, Yang XH. Informing the improvement and biodesign of crassulacean acid metabolism via system dynamics modelling. New Phytologist 2013, 200(4), 946-949.
• Tzortzakis N, Taybi T, Antony E, Singleton I, Borland A, Barnes J. Profiling shifts in protein complement in tomato fruit induced by atmospheric ozone-enrichment and/or wound-inoculation with Botrytis cinerea. Postharvest Biology and Technology 2013, 78, 67-75.
• Haider MS, Barnes JD, Cushman JC, Borland AM. A CAM- and starch-deficient mutant of the facultative CAM species Mesembryanthemum crystallinum reconciles sink demands by repartitioning carbon during acclimation to salinity. Journal of Experimental Botany 2012, 63(5), 1985-1996.
• Ceusters J, Borland AM, Godts C, Londers E, Croonenborghs S, Van Goethem D, De Proft MP. Crassulacean acid metabolism under severe light limitation: a matter of plasticity in the shadows?. Journal of Experimental Botany 2011, 62(1), 283-291.
• Tzortzakis N, Taybi T, Roberts R, Singleton I, Borland A, Barnes J. Low-level atmospheric ozone exposure induces protection against Botrytis cinerea with down-regulation of ethylene-, jasmonate- and pathogenesis-related genes in tomato fruit. Postharvest Biology and Technology 2011, 61(2-3), 152-159.
• Tzortzakis N, Taybi T, Roberts R, Singleton I, Borland A, Barnes J. Low-level atmospheric ozone exposure induces protection against Botrytis cinerea with down-regulation of ethylene-, jasmonate- and pathogenesis-related genes in tomato fruit. Postharvest Biology and Technology 2011, 61(2-3), 152-159.
• Borland AM, Zambrano VAB, Ceusters J, Shorrock K. The photosynthetic plasticity of crassulacean acid metabolism: an evolutionary innovation for sustainable productivity in a changing world. New Phytologist 2011, 191(3), 619-633.
• Goumenaki E, Taybi T, Borland A, Barnes J. Mechanisms underlying the impacts of ozone on photosynthetic performance. Environmental and Experimental Botany 2010, 69(3), 259-266.
• Ceusters J, Borland AM, Ceusters N, Verdoodt V, Godts C, De Proft MP. Seasonal influences on carbohydrate metabolism in the CAM bromeliad Aechmea 'Maya': consequences for carbohydrate partitioning and growth. Annals of Botany 2010, 105(2), 301-309.
• Ceusters J, Borland AM, Londers E, Verdoodt V, Godts C, De Proft MP. Differential usage of storage carbohydrates in the CAM bromeliad Aechmea 'Maya' during acclimation to drought and recovery from dehydration. Physiologia Plantarum 2009, 135(2), 174-184.
• Ceusters J, Borland AM, De Proft MP. Drought adaptation in plants with crassulacean acid metabolism involves the flexible use of different storage carbohydrate pools. Plant Signaling and Behavior 2009, 4(3), 212-214.
• Borland AM, Griffiths H, Hartwell J, Smith JAC. Exploiting the potential of plants with crassulacean acid metabolism for bioenergy production on marginal lands. In: Journal of Experimental Botany: Workshop on Plant Biomass for Food and Energy. 2009, Baeza, Spain: Oxford University Press.
• Antony E, Taybi T, Courbot M, Mugford ST, Smith JAC, Borland AM. Cloning, localization and expression analysis of vacuolar sugar transporters in the CAM plant Ananas comosus (pineapple). In: 14th International Congress of Photosynthesis. 2008, Glasgow, UK: Oxford University Press.
• Ceusters J, Borland AM, Londers E, Verdoodt V, Godts C, De Proft MP. Diel shifts in carboxylation pathway and metabolite dynamics in the CAM bromeliad Aechmea 'Maya' in response to elevated CO2. Annals of Botany 2008, 102(3), 389-397.
• Cushman JC, Agarie S, Albion RL, Elliot SM, Taybi T, Borland AM. Isolation and characterization of mutants of common ice plant deficient in Crassulacean acid metabolism. Plant Physiology 2008, 147(1), 228-238.
• Antony E, Borland AM. The role and regulation of sugar transporters in plants with Crassulacean acid metabolism. In: U. Luttge, W. Beyschlag, J. Murata, ed. Progress in Botany. Germany: Springer, 2008, pp.127–143.
• Niewiadomska E, Borland AM. Crassulacean acid metabolism: a cause or consequence of oxidative stress in planta?. In: Luttge, UE; Beyschlag, W; Murata, J, ed. Progress in Botany. Berlin Heidelberg: Springer, 2007, pp.247-266.
• Tzortzakis N, Borland A, Singleton I, Barnes J. Impact of atmospheric ozone-enrichment on quality-related attributes of tomato fruit. Postharvest Biology and Technology 2007, 45(3), 317-325.
• Borland A, Elliott S, Patterson S, Taybi T, Cushman J, Pater B, Barnes J. Are the metabolic components of crassulacean acid metabolism up-regulated in response to an increase in oxidative burden?. In: Meeting on Phenotypic Plasticity and the Changing Environment held at the Society for Experimental Biology Plant Frontiers Meeting. 2006, Sheffield: Journal of Experimental Botany, Oxford University Press.
• Hale ML, Borland AM, Wolff K. High degree of conservation of nuclear microsatellite loci in the genus Clusia. Genome 2005, 48(5), 946-950.
• Hale ML, Borland AM, Gustafsson MHG, Wolff K. Causes of Size Homoplasy Among Chloroplast Microsatellites in Closely Related Clusia Species. Journal of Molecular Evolution 2004, 58(2), 182- 190.
• Taybi T, Nimmo HG, Borland AM. Expression of phosphoenolpyruvate carboxylase and phosphoenolpyruvate carboxylase kinase genes. Implications for genotypic capacity and phenotypic plasticity in the expression of crassulacean acid metabolism. Plant Physiology 2004, 135(1), 587-598.
• Borland AM, Taybi T. Synchronization of metabolic processes in plants with Crassulacean acid metabolism. Journal of Experimental Botany 2004, 55(400), 1255-1265.
• Dodd AN, Griffiths H, Taybi T, Cushman JC, Borland AM. Integrating diel starch metabolism with the circadian and environmental regulation of Crassulacean acid metabolism in Mesembryanthemum crystallinum. Planta 2003, 216(5), 789-797.
• Haslam R, Borland A, Maxwell K, Griffiths H. Physiological responses of the CAM epiphyte Tillandsia usneoides L. (Bromeliaceae) to variations in light and water supply. Journal of Plant Physiology 2003, 160(6), 627-634.
• Borland AM, Dodd AN. Carbohydrate partitioning in crassulacean acid metabolism plants: Reconciling potential conflicts of interest. Functional Plant Biology 2002, 29(6), 707-716.
• Dodd AN, Borland AM, Haslam RP, Griffiths H, Maxwell K. Crassulacean acid metabolism: plastic, fantastic. Journal of Experimental Botany 2002, 53(369), 569-580.
• Taybi T, Cushman JC, Borland AM. Environmental, hormonal and circadian regulation of crassulacean acid metabolism expression. In: 3rd International Congress on Crassulacean Acid Metabolism. 2002, Coconut Beach, Australia: Functional Plant Biology, CSIRO Publishing.
• Cushman JC, Borland AM. Induction of Crassulacean acid metabolism by water limitation. Plant, Cell and Environment 2002, 25(2), 295-310.
• Hale ML, Squirrell J, Borland AM, Wolff K. Isolation of polymorphic microsatellite loci in the genus Clusia (Clusiaceae). Molecular Ecology Notes 2002, 2(4), 506-508.
• Griffiths H, Helliker B, Roberts A, Haslam RP, Girnus J, Robe WE, Borland AM, Maxwell K. Regulation of Rubisco activity in crassulacean acid metabolism plants: better late than never. In: Functional Plant Biology: 3rd International Congress on Crassulacean Acid Metabolism. 2002, Coconut Beach, Australia: CSIRO Publishing.
• Haslam RP, Borland AM, Griffiths H. Short-term plasticity of crassulacean acid metabolism expression in the epiphytic bromeliad, Tillandsia usneoides. In: Functional Plant Biology: 3rd International Congress on Crassulacean Acid Metabolism. 2002, Coconut Beach, Australia: CSIRO Publishing.
• Gehrig HH, Winter K, Cushman J, Borland A, Taybi T. An Improved RNA Isolation Method for Succulent Plant Species Rich in Polyphenols and Polysaccharides. Plant Molecular Biology Reporter 2000, 18(4), 369-376.
• Barnes J, Bender J, Lyons T, Borland A. Natural and man-made selection for air pollution resistance. Journal of Experimental Botany 1999, 50(338), 1423-1435.