Staff Profile

Introduction

I joined the University as a research associate in 1987 and held a personal NERC fellowship from 1990-1994. I was appointed as Lecturer in Plant Biochemistry in 1998 and was awarded a personal readership in 2003. I held a joint appointment with the Oak Ridge National Laboratory in the US (2012-2018) and was awarded a personal chair in Plant Physiology at Newcastle in 2013.

Qualifications

• BSc (Hons) Botany, University of Glasgow
• PhD University College North Wales

Previous Positions

• NERC Fellow 1990-1994
• Visiting Lecturer, University Sunderland

External Appointments

• Joint faculty appointment at the Oak Ridge National Laboratory, TN, USA 
• Gatsby Plant Science Mentor
• Subject External Examiner for BSc Plant Biology and MSc Plant Biology and Biotechnology, University College Dublin (2016-2019)
• External Examiner for BSc Biological Sciences, University of Essex, (2018-2021)
• Fellow of the Royal Society of Biology
• Board of Editors Global Change Biology: Bioenergy.

Area of Expertise

Photosynthetic carbon assimilation, crassulacean acid metabolism

Google scholar page

Research Interests

My research focusses on a specialised mode of photosynthesis, crassulacean acid metabolism (CAM), which 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 permits the uptake of CO2 at night and has evolved in up to 7% of higher plants, primarily as an adaptation to water-limited habitats. The expression of CAM is readily modulated by the environment, and thus serves as a model system for establishing the functional significance of genes and enzymes that optimize physiological performance in arid, resource-limited habitats. The day/night separation of carboxylation processes in the photosynthetic cells of CAM plants, also poses fundamental questions in terms of metabolic control and circadian synchronization of metabolism.

The drivers of my research are to understand the molecular and metabolic basis of CAM in its various physiological manifestations and to use this information to exploit the potential of naturally evolved and engineered CAM for sustainable productivity in a warmer and drier world.

Selected recent publications

Ceusters N, Ceusters J, Hurtado-Castano N, Dever LV, Boxall SF, Kneřová, J, Waller JL, Rodick R, Van Den Ende W, Hartwell J, Borland AM. (2021) Phosphorolytic degradation of leaf starch via plastidic α-glucan phosphorylase leads to optimized plant growth and water use efficiency over the diel phases of Crassulacean acid metabolism. Journal of Experimental Botany 72, 4419-4434.            

Ceusters N, Borland AM, Ceusters J. (2021) How to resolve the enigma of diurnal malate remobilisation from the vacuole in plants with crassulacean acid metabolism? New Phytologist 229, 3116-3124.

Liu D, Hu R. Zhang J, Guo H-B, Cheng H, Li L, Borland AM, Qin H, Chen J-G, Muchero W, Tuskan GA, Yang X.(2021) Overexpression of an Agave Phosphoenolpyruvate Carboxylase Improves Plant Growth and Stress Tolerance. Cells 10 (3), 582.

Leverett A, Hurtado Castaño N, Ferguson K, Winter K, Borland AM. (2021) Crassulacean acid metabolism (CAM) supersedes the turgor loss point (TLP) as an important adaptation across a precipitation gradient, in the genus Clusia Functional Plant Biology 48, 703-716.

Abraham PE, Hurtado-Castano N, Cowan-Turner D, Barnes JD, Poudel S, Hettich R, Santelia D, Borland AM (2020) Peeling back the layers of crassulacean acid metabolism: functional differentiation between epidermis and mesophyll of Kalanchoë fedstchenkoi. Plant Journal 103, 869-888

Zhang J, Hu R, Sreedasyam A, Garcia TM, Lipzen A, Wang M, Yerramsetty P, Liu D, Ng V, Schmutz J, Cushman JC, Borland AM, Pasha A, Provart NJ, Chen J-G, Muchero W, Tuskan GA, Yang X. (2020) Light-responsive expression atlas reveals the effects of light quality and intensity in Kalanchoë fedtschenkoi, a plant with crassulacean acid metabolism. GigaScience, 9, art. no. giaa018

Heyduk K, Ray JR, Ayyampalayam S, Moledina N, Borland A, Harding S, Tsai C-J, Leebens Mack J (2019) Nocturnal expression of Crassulacean acid metabolism (CAM) genes predates the origin of CAM in the genus Yucca. Journal of Experimental Botany 70, 6597-6609

Yin H, Weston D, Ranjan P, Abraham P, Jawdy S, Tuskan G, Tschaplinski T, Wullschleger S, Hettich R, Guo H-B, Huo H, Borland A, Wachira J, Gross S, Wang Z, Visel A, Yang X (2018) Diel rewiring and positive selection of ancient plant proteins enabled evolution of CAM photosynthesis in Agave. BMC Genomics 19, 588

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. 

Undergraduate Teaching

Stage 3:

Global challenges for Plant Science Research (BIO3052 Module Leader)

• Articles

  • Leverett A, Hartzell S, Winter K, Garcia M, Aranda J, Virgo A, Smith A, Focht P, Rasmussen-Arda A, Willats WGT, Cowan-Turner D, Borland AM. Dissecting succulence: Crassulacean acid metabolism and hydraulic capacitance are independent adaptations in Clusia leaves. Plant Cell and Environment 2023, 46(5), 1472-1488.
  • Fradera-Soler M, Leverett A, Mravec J, Jorgensen B, Borland AM, Grace OM. Are cell wall traits a component of the succulent syndrome?. Frontiers in Plant Science 2022, 13, 1043429.
  • Liu D, Hu R, Zhang J, Guo H-B, Cheng H, Li L, Borland AM, Qin H, Chen J-G, Muchero W, Tuskan GA, Yang X. Overexpression of an Agave Phosphoenolpyruvate Carboxylase Improves Plant Growth and Stress Tolerance. Cells 2021, 10(3), 582.
  • Ceusters N, Borland AM, Ceusters J. How to resolve the enigma of diurnal malate remobilisation from the vacuole in plants with crassulacean acid metabolism?. New Phytologist 2021, 229(6), 3116-3124.
  • Abraham PE, Hurtado Castano N, Cowan-Turner D, Barnes J, Poudel S, Hettich R, Flutsch S, Santelia D, Borland AM. Peeling back the layers of crassulacean acid metabolism: functional differentiation between Kalanchoë fedtschenkoi epidermis and mesophyll proteomes. Plant Journal 2020, 103(2), 869-888.
  • Heyduk K, Ray JN, Ayyampalayam S, Moledina N, Borland A, Harding SA, Tsai C-J, Leebens-Mack J. Shared expression of Crassulacean acid metabolism (CAM) genes predates the origin of CAM in the genus Yucca. Journal of Experimental Botany 2019, 70(22), 6597-6609.
  • Yin H, Guo H-B, Weston DJ, Borland AM, Ranjan P, Abraham PE, Jawdy SS, Wachira J, Tuskan GA, Tschaplinski TJ, Wullschleger SD, Guo H, Hettich RL, Gross SM, Wang Z, Visel A, Yang X. Diel rewiring and positive selection of ancient plant proteins enabled evolution of CAM photosynthesis in Agave. BMC Genomics 2018, 19, 588.
  • 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.
  • 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.
  • 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.
  • 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.
  • 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.
  • 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.
  • 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.
  • 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.
  • 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.
  • 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.
  • 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.
  • 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.
  • 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.
  • 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, 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.
  • 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.
  • 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.
  • 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.
  • 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.
  • Hale ML, Borland AM, Wolff K. High degree of conservation of nuclear microsatellite loci in the genus Clusia. Genome 2005, 48(5), 946-950.
  • Borland AM, Taybi T. Synchronization of metabolic processes in plants with Crassulacean acid metabolism. Journal of Experimental Botany 2004, 55(400), 1255-1265.
  • 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.
  • 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.
  • 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.
  • 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.
  • 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.
  • Borland AM, Dodd AN. Carbohydrate partitioning in crassulacean acid metabolism plants: Reconciling potential conflicts of interest. Functional Plant Biology 2002, 29(6), 707-716.
  • 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.

• Book Chapters

  • 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.

• Conference Proceedings (inc. Abstracts)

  • 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.
  • 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.
  • 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.
  • 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.
  • 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.

• Editorials

  • Yang X, Cushman JC, Borland AM, Liu Q. Editorial: Systems Biology and Synthetic Biology in Relation to Drought Tolerance or Avoidance in Plants. Frontiers in Plant Science 2020, 11, 394.
  • 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, Yang XH. Informing the improvement and biodesign of crassulacean acid metabolism via system dynamics modelling. New Phytologist 2013, 200(4), 946-949.

• Note

  • Yin H, Guo H-B, Weston DJ, Borland AM, Ranjan P, Abraham PE, Jawdy SS, Wachira J, Tuskan GA, Tschaplinski TJ, Wullschleger SD, Guo H, Hettich RL, Gross SM, Wang Z, Visel A, Yang X. Correction to: Diel rewiring and positive selection of ancient plant proteins enabled evolution of CAM photosynthesis in Agave . BMC Genomics 2019, 20(1), 279.

• Reviews

  • 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.
  • 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.
  • 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, 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.
  • 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.
  • 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.
  • 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.
  • Cushman JC, Borland AM. Induction of Crassulacean acid metabolism by water limitation. Plant, Cell and Environment 2002, 25(2), 295-310.
  • Dodd AN, Borland AM, Haslam RP, Griffiths H, Maxwell K. Crassulacean acid metabolism: plastic, fantastic. Journal of Experimental Botany 2002, 53(369), 569-580.