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Cristina Maria Nobre Sobral de Vilhena da Cruz Houghton

Posted by | February 28, 2021


Cristina Maria Nobre Sobral de Vilhena da Cruz Houghton

Job Title:

Professor auxiliar


Phone Number:



Google Scholar Profile


I am interested in the physiological mechanisms that determine the suitability of terrestrial plants to their environments, especially in environments rich in ammonium.

My main scientific interest is the physiological ecology of nitrogen (N) acquisition and impacts of increased N availability on terrestrial plants. The distinct effects of NO3- and NH4+ on plant performance and species preference for one of these chemical species of N have been a constant in my research. I am examining the role of plant N fluxes in several key areas: ecological succession, primary productivity, carbon nitrogen interactions, physiology of inorganic nitrogen assimilation and the role of plant micro-organism interactions in nitrogen acquisition. Special attention is given to rhizospheric microbial consortia (free living N fixers, phosphate solubilizers and arbuscular mycorrhizal fungi) in nitrogen acquisition, the mechanisms and fluxes involved are part of the research programme.

My current research is driven by three overarching objectives:

  • to maintain long-term ecological experiments in order to collect data on the response of Mediterranean ecosystems to changes in resource availability over time and space;
  • to understand the role of soil ecology on plant productivity and sustainability of eco- and agro-systems;
  • to engineer the rhizosphere of crop plants in order to obtain plants tolerant of higher stresses, with increased nutrient use efficiencies and nutritional value.

The approach is highly multidisciplinary, ranging from biochemical processes to field ecological analyses. Techniques include enzymatic kinetics, net flux kinetics, ionic and metabolic profiling of tissues, and growth analysis. The biological systems used are carob (Ceratonia siliqua L.), Arabidopsis thaliana and in vitro arbuscular mycorrhizal fungi cultures. New projects are considering the physiology of the endophyte Piriformospora indica and its application as a biofertilizer in order to maintain food security and environmental sustainability.


Research Areas:

  • Nitrogen metabolism and use efficiency

Current N-related Projects:

  • BioClub
  • BioInvent
  • Novinoc


Dias T, Crous CJ, Liberati D, Munzi S, Gouveia C, Ulm F, Afonso AC, Ochoa-Hueso R, Manrique E, Sheppard L, Martins-Loução MA, Bernardes da Silva A, Cruz C. Alleviating nitrogen limitation in Mediterranean maquis vegetation leads to ecological degradation. Land Degradation & Development. Published online, 2017. DOI:10.1002/ldr.2784 (IF 9.787).

Fonseca MB, Dias T, Carolino MM, França MGC, Cruz C. Belowground microbes mitigate plant- plant competition. Plant Science. 2017;262:175-181. DOI:10.1016/j.plantsci.2017.06.006 (IF 3.437).

Hessini K, Kronzucker HJ, Abdelly C, Cruz C. Drought stress obliterates the preference for ammonium as an N source in the C4 plant Spartina alterniflora. Journal of Plant Physiology. 2017;213:98-107. DOI:10.1016/j.jplph.2017.03.003 (IF 2.97).

Munzi S, Cruz C, Maia R, Máguas C, Perestrello-Ramos MM, Branquinho C. Intra- and inter- specific variations in chitin in lichens along a N-deposition gradient. Environmental Science and Pollution Research. Published online, 2017. DOI:10.1007/s11356-017-0378-3 (IF 2.741).

Munzi S, Sheppard LJ, Leith ID, Cruz C, Branquinho C, Bini L, Gagliardi A, Cai G, Parrotta L. The cost of surviving nitrogen excess: energy and protein demand in the lichen Cladonia portentosa as revealed by proteomic analysis. Planta. 2017;245:819-833. DOI:10.1007/s00425-017-2647-2 (IF 3.239).

Ochoa-Hueso R, Munzi S, Alonso R, Arróniz-Crespo M, Avila A, Bermejo V, Bobbink R, Branquinho C, Concostrina-Zubiri L, Cruz C, Cruz de Carvalho R, De Marco A, Dias T, Elustondo D, Elvira S, Estébanez B, Fusaro L, Gerosa G, Izquieta-Rojano S, Lo Cascio M, Marzuoli R, Matos P, Mereu S, Merino J, Morillas L, Nunes A, Paoletti E, Paoli L, Pinho P, Rogers IB, Santos A, Sicard P, Stevens CJ, Theobald MR. Ecological Impacts of Atmospheric Pollution and Interactions with Climate Change in Terrestrial Ecosystems of the Mediterranean Basin: Current Research and Future Directions. Environmental Pollution. 2017;227:194-206. DOI:10.1016/j.envpol.2017.04.062 (IF 4.839).

Rai A, Cherif A, Cruz C, Nabti E. Extracts from seaweeds and opuntia ficus-indica cladodes enhance diazotrophic-PGPR halotolerance, their enzymatic potential, and their impact on wheat germination under salt stress. Pedosphere. Published online, 2017. DOI:10.1016/S1002- 0160(17)60333-3 (IF 1.734).

Santana MM, Gonzalez JM, Cruz C. Nitric Oxide Accumulation: The Evolutionary Trigger for Phytopathogenesis. Frontiers in Microbiology. 2017;8:1947. DOI:10.3389/fmicb.2017.01947 (IF 4.076).

Ulm F, Gouveia C, Dias T, Cruz C. N fertilization in a Mediterranean ecosystem alters N and P turnover in soil, roots and the ectomycorrhizal community. Soil Biology and Biochemistry. 2017;113:60-70. DOI:10.1016/j.soilbio.2017.05.028 (IF 4.152).

Ulm F, Hellmann C, Cruz C, Máguas C. N/P imbalance as a key driver for the invasion of oligotrophic dune systems by a woody legume. Oikos. 2017;126:231-240. DOI:10.1111/oik.03810 (IF 3.586).

Ulm F, Jacinto J, Cruz C, Máguas C. How to outgrow your native neighbour? Belowground changes under native shrubs at an early stage of invasion. Land Degradation & Development. Published online, 2017. DOI:10.1002/ldr.2768 (IF 9.787).

Canton GC, Bertolazi AA, Cogo AJD, Eutrópio FJ, Melo J, Souza SB, Krohling CA, Campostrini E, Silva AG, Façanha AR, Sepúlveda N, Cruz C, Ramos AC. Biochemical and ecophysiological responses to manganese stress by ectomycorrhizal fungus Pisolithus tinctorius and in association with Eucalyptus grandis. Mycorrhiza. 2016;26:475-487. DOI:10.1007/s00572-016-0686-3 (IF 3.459).

Esteban R, Ariz I, Cruz C, Moran JF. Review: Mechanisms of ammonium toxicity and the quest for tolerance. Plant Science. 2016;248:92-101. DOI:10.1016/j.plantsci.2016.04.008 (IF 3.607).

Godinho DP, Janssen A, Dias T, Cruz C, Magalhães S. Down-regulation of plant defence in a resident spider mite species and its effect upon con- and heterospecifics. Oecologia. 2016;180:161-167. DOI: 10.1007/s00442-015-3434-z (IF 3.093).

Hamouda I, Badri M, Mejri M, Ferchichi S, Cruz C, Siddique KHM, Hessini K. Salt tolerance of Beta macrocarpa is associated with efficient osmotic adjustment and increased apoplastic water content. Plant Biology. 2016;18:369–375. DOI:10.1111/plb.12419 (IF 2.633).

Melo, J; Carolino, M; Carvalho, L; Correia, P; Tenreiro, R; Chaves, S; Meleiro, AI; de Souza, SB; Dias, T; Cruz, C; Ramos AC. Crop management as a driving force of plant growth promoting rhizobacteria physiology. SpringerPlus. 2016;5:1574. DOI:10.1186/s40064-016-3232-z (IF 0.982).

Munzi S, Cruz C, Selosse MA, Rodriguez R. Symbiotic lifestyle – 8th International Symbiosis Society (ISS) congress, Lisbon (Portugal), 12–18 July 2015. Symbiosis. 2016;68:1-3. DOI:10.1007/s13199-016-0393-z (IF 1.438).

Rainha N, Medeiros VP, Câmara M, Faustino H, Leite JP, Barreto MC, Cruz C, Pacheco CA, Ponte D, Bernardes da Silva A. Plasticity of Crassulacean Acid Metabolism at subtropical latitudes: the pineapple case study. Physiologia Plantarum 2016;156:29-39. DOI:10.1111/ppl.12386 (IF 3.138).

Rainha N, Medeiros VP, Ferreira C, Raposo A, Leite JP, Cruz C, Pacheco CA, Ponte D, Silva AB. Leaf malate and succinate accumulation are out of phase in the CAM plant Ananas comosus. Plant Physiology and Biochemistry. 2016;100:47-51. DOI:10.1016/j.plaphy.2015.12.021 (IF 2.756).

Ariz I, Cruz C, Neves T, Irigoyen JJ, García C, Nogués S, Aparicio-Tejo PM and Aranjuelo I. Leaf δ15N as a physiological indicator of the responsiveness of N2-fixing alfalfa plants to elevated [CO2], temperature and low water availability. Frontiers in Plant Science. 2015;6:574. DOI:10.3389/fpls.2015.00574 (IF 3.9).

Corrêa A, Cruz C, Ferrol N. Nitrogen and Carbon/Nitrogen dynamics in arbuscular mycorrhiza: the great unknown. Mycorrhiza. 2015;25:499-515. DOI:10.1007/s00572-015-0627-6 (IF 2.985).

Dias T, Martins-Loução MA, Sheppard L, Cruz C. Plant tolerance of ammonium varies between co-existing Mediterranean species. Plant and Soil. 2015;395:243-252. DOI:10.1007/s11104-015- 2552-z (IF 2.952).

Hessini K, Ferchichi S, Ben Youssef S, Werner KH, Cruz C, Gandour M. How Does Salinity Duration Affect Growth and Productivity of Cultivated Barley? Agronomy Journal. 2015;107:174-180. DOI:10.2134/agronj14.0281. (IF 1.542).

Shibata H, Branquinho C, McDowell WH, Mitchell MJ, Monteith DT, Tang J, Arvola L, Cruz C, Cusack D, Halada L, Kopacek J, Máguas C, Sajidu S, Schubert H, Tokuchi N, Záhora J. Consequence of altered nitrogen cycles in the coupled human and ecological system under changing climate: the need for long-term and site-based research. Ambio. 2015;44:178-193. DOI:10.1007/s13280-014-0545-4 (IF 2.295).

Shvaleva A, Siljanen HM, Correia A, Costa E Silva F, Lamprecht R, Lobo-do-Vale R, Bicho MG, Fangueiro D, Anderson M, Pereira JS, Chaves M, Cruz C, Martikainen PJ. Environmental and microbial factors influencing methane and nitrous oxide fluxes in Mediterranean cork oak woodlands: trees make a difference. Frontiers in Microbiology. 2015;6:1104. DOI:10.3389/fmicb.2015.01104 (IF 3.941).

Corrêa A, Cruz C, Pérez-Tienda J, Ferrol N. Shedding light onto nutrient responses of arbuscular mycorrhizal plants: nutrient interactions may lead to unpredicted outcomes of the symbiosis. Plant Science. 2014;221-222:29-41. DOI:10.1016/j.plantsci.2014.01.009 (IF 2.922).

Dias T, Clemente A, Martins-Loução MA, Sheppard L, Bobbink R, Cruz C. Ammonium as a driving force of plant diversity and ecosystem functioning: observations based on 5 years’ manipulation of N dose and form in a Mediterranean ecosystem. PLoS One. 2014;9:e92517. DOI:10.1371/journal.pone.0092517 (IF 3.73).

Fonseca MB, Carolino MMSSL, Dias T, Cruz C, França MGC. Early growth of Brazilian tree Dimorphandra wilsonii is also threatened by African grass Urochloa decumbens. Journal of Plant Interactions. 2014;9:92-99. DOI:10.1080/17429145.2013.770085 (IF 0.641).

Gouveia W, Jorge T, Martins S, Meireles M, Carolino M, Cruz C, Almeida TV, Araújo MEM. Toxicity of ionic liquids prepared from biomaterials. Chemosphere. 2014;104:51–56. DOI:10.1016/j.chemosphere.2013.10.055. (IF 3.137).

Munzi S, Cruz C, Branquinho C, Pinho P, Leith ID, Sheppard LJ. Can ammonia tolerance amongst lichen functional groups be explained by physiological responses? Environmental Pollution. 2014;187:206–209. DOI:10.1016/j.envpol.2014.01.009 (IF 3.73).

Pinho P, Llop E, Ribeiro MC, Cruz C, Soares A, Pereira MJ, Branquinho C. Tools for determining critical levels of atmospheric ammonia under the influence of multiple disturbances. Environmental Pollution. 2014;188:88-93. DOI:10.1016/j.envpol.2014.01.024 (IF 3.73).

Shvaleva A, Costa e Silva F, Costa JM, Anderson M, Lobo-do-Vale R, Fangueiro D, Bicho C, Pereira JS, Chaves MM, Skiba U, Cruz C. Comparison of methane, nitrous oxide fluxes and CO2 respiration rates from a Mediterranean cork oak ecosystem and improved pasture. Plant and Soil. 2014;374:883-898. DOI:10.1007/s11104-013-1923-6. (IF 2.638).

Silva MCS, Paula TA, Moreira BC, Carolino M, Cruz C, Bazzolli DMS, Silva CC, Kasuya MCM. Nitrogen-fixing bacteria in Eucalyptus globulus plantations. PLoSOne. 2014;9:e111313. DOI:10.1371/journal.pone.0111313 (IF 3.53).

Baptista SL, Vaz Pinto P, Freitas MC, Cruz C, Palmeirim JM. Geophagy by African ungulates: the case of the critically endangered giant sable antelope of Angola (Hippotragus niger variani). African Journal of Ecology. 2013;51:139–146. DOI:10.1111/aje.12020. (IF 0.631).

Dias T, Oakley S, Alarcón-Gutiérrez E, Ziarelli F, Trindade H, Martins-Loução MA, Sheppard L, Ostle N, Cruz C. N-driven changes in a plant community affect leaf-litter traits and may delay organic matter decomposition in a Mediterranean maquis. Soil Biology and Biochemistry. 2013;58:163–171. DOI:10.1016/j.soilbio.2012.10.027 (IF 3.504).

Ekblad A, Wallander H, Godbold DL, Johnson D, Baldrian P, Björk RG, Cruz C, Epron D, Kieliszewska-Rokicka B, Kjöller R, Kraigher H, Matzner E, Neumann J, Plassard C. The production and turnover of extramatrical mycelium of ectomycorrhizal fungi in forest soils: role in carbon cycling. Plant and Soil. 2013;366:1-27. DOI:10.1007/s11104-013-1630-3 (IF 2.638).

Hessini K, Ben Hamed K, Gandour M, Mejry M, Abdelly C, Cruz C. Ammonium nutrition in the halophyte Spartina alterniflora under salt stress: evidence for a priming effect of ammonium? Plant and Soil. 2013;370:163-173. DOI:10.1007/s11104-013-1616-1. (IF 2.638).

Munzi S, Branquinho C, Cruz C, Loppi S. Nitrogen tolerance in the lichen Xanthoria parietina: the sensitive side of a resistant species. Functional Plant Biology. 2013;40:237-243. DOI:10.1071/FP12127 (IF 2.929).

Pintó-Marijuan M, Bernardes da Silva A, Flexas J, Dias T, Zarrouk O, Martins-Loução MA, Chaves MM, Cruz C. Photosynthesis of Quercus suber is affected by atmospheric NH3 generated by multifunctional agrosystems. Tree Physiology. 2013;33:1328-1337. DOI:10.1093/treephys/tpt077. (IF 2.853).

Corrêa A, Gurevitch J, Martins-Loução MA, Cruz C. C allocation to the fungus is not a cost to the plant in ectomycorrhizae. OIKOS. 2012;121:449–463. DOI:10.1111/j.1600-0706.2011.19406.x (IF 3.393).

Dias T, Martins-Loução MA, Sheppard L, Cruz C. The strength of the biotic compartment in retaining nitrogen additions prevents nitrogen losses from a Mediterranean maquis. Biogeosciences. 2012;9:193-201. DOI:10.5194/bg-9-193-2012 (IF 3.587).