Phosphorus-Acquisition and Phosphorus-Conservation Mechanisms of Plants Native to South-Western Australia Or to Brazilian Rupestrian Fields

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Phosphorus-Acquisition and Phosphorus-Conservation Mechanisms of Plants Native to South-Western Australia Or to Brazilian Rupestrian Fields Phosphorus-acquisition and phosphorus-conservation mechanisms of plants native to south-western Australia or to Brazilian rupestrian fields Mariana Cruz Rodrigues de Campos MSc in Plant Biology This thesis is presented for the degree of Doctor of Philosophy of Plant Biology of The University of Western Australia The University of Western Australia Faculty of Natural and Agricultural Sciences School of Plant Biology 2011 2 ACKNOWLEDGEMENTS I would like to thank my supervisors; Dr Hans Lambers, Dr Rafael Silva Oliveira and Dr Stuart James Pearse for all the advice, support and encouragement during my PhD. The suggestions made by the thesis examiners, Dr Michelle Watt and Dr Rebecca Ostertag were extremely valuable and much appreciated. For helping me with key concepts and methodologies, I thank Dr Erik Veneklaas, Dr Mark Brundrett, Dr Michael Shane and Tamara Edmonds-Tibbett. I’d also like to acknowledge all administrative and support staff in the School of Plant Biology for the everyday work of keeping things running so I’d be allowed to focus on my thesis. During my field work in Brazil, the supervision of Dr Rafael S. Oliveira allowed for the work to be much more efficient and targeted. His help and that of (unpaid) friends were absolutely essential and I truly appreciate and hope one day to repay Ana Luíza Muler, Maria Cecília Alvim Penteado, Hugo Galvão and Caio Guilherme Pereira. I’d also like to thank the taxonomists who helped with the identification of the material collected in Brazil: Juliana Souza Silva (for the identification of Fabaceae), Marcelo Trovó (Eriocaulaceae), Maria das Graças Lapa Wanderley (Xyridaceae) and Dr Renato de Mello-Silva (Velloziaceae). As my work progressed, I always had somebody giving me a good suggestion or helping me find solutions to my problems. The list of people who contributed in this way is much too long, but a special mention goes to the Plant Biology tea club members and to the glasshouse staff. I extend my appreciation to the funding bodies that have financed me in my PhD research. Thanks to the University of Western Australia and the School of Plant Biology, I received a scholarship. The equipment, materials, travelling and attendance to conferences were made possible with the funding from Plant Biology Research Grant (2008-2011); ANZ Holsworth Wildlife Foundation Grant (2008, 2009, 2010); Brazilian National Research Council, CNPq (2008) and Mary Janet Lindsay of Yanchep Memorial Fund (2010). My appreciation is extended to the directors and administrative staff of the field sites in which I worked in, both in Australia (Bold Park, Botanic Gardens & Parks Authority) and in Brazil (Santuário do Caraça, Propriedade Particular da Província Brasileira da 3 Congregação da Missão; Parque Nacional da Serra do Cipó; Parque Estadual do Rio Preto; and Parque Estadual da Serra do Cabral). Finally, I thank my parents, family and friends in Brazil for supporting me in the decision of moving abroad; and for their continuous presence in my life, giving me comfort and love. Thanks also to those friends in Australia who have made me feel so welcome and happy and above all, to the never-ending support and encouragement of my very patient partner Troy. 4 5 SUMMARY Phosphorus (P) is an essential macronutrient for life and it has been widely recognised as one of the most limiting nutrients for plant growth. The vast majority of P in the soil originates from the parent rock, and over prolonged periods of time, it is lost from the system due to weathering and leaching. This is the reason why P is particularly limiting in old soils, such as in the kwongan in the south-west of Australia; the fynbos in the Cape floristic region in South Africa, and the rupestrian fields in central Brazil. The study of P acquisition by native plants is of great importance, because these plants have evolved mechanisms and strategies to thrive under low availability of P; conditions in which crop species would not survive. Studying and understanding P-acquisition and P- conservation traits of native plants in their P-impoverished environments, is taking a step towards decreasing fertiliser use in crops and minimising its detrimental environmental consequences. This thesis aims to deepen the understanding of P-acquisition and P-conservation mechanisms by addressing three aspects that were, until now, gaps in ecophysiology (chapter 1). Through field work (chapter 2), I have compared and contrasted already well known P- impoverished environments to a much less studied and explored area: the rupestrian fields in central Brazil. Leaf nutrient resorption and root specialisations were the focus of the field work at nine sites in Brazil. I discovered that the species that occupy the rupestrian fields are taxonomically very distinct from those in the south-west of Australia, but that there is a functional convergence. I discuss the root specialisations found (root clusters and cluster-like, sand-binding roots, mycorrhizal associations and dense root hairs) and their relationship to soil fertility and the varying degrees of P resorption from senescing leaves. Apart from this exploratory field work, I have also investigated how two different but co-occurring specialisations towards enhanced P-acquisition (cluster roots and mycorrhizal associations) are related to each other, to P supply and to the internal P concentration of an Australian native legume, Viminaria juncea (chapter 3). This waterlogging-tolerant species was found to be unique in that it maintains stable shoot P concentrations independent of P supply. As a consequence of the steady shoot P concentration, the suppression of mycorrhizal colonisation and cluster root formation was only marginal. 6 In addition, I have experimentally tested whether net P-uptake capacity is correlated with leaf P-resorption efficiency of species native to the Perth region, south-western Australia (chapter 4). My results indicate there is an inverse relationship between the capacity to down-regulate net P uptake and the P-resorption efficiency for Acacia truncata and A. xanthina (Fabaceae), as well as for Banksia attenuata, B. menziesii and Hakea prostrata (Proteaceae). Both Acacia species were able to down-regulate P-uptake capacity, but less efficient at remobilising P from senescing leaves. The three Proteaceae species were unable to down-regulate P-uptake capacity which led to P- toxicity symptoms, but on the other hand, they are extremely efficient and proficient at P-resorption. P-impoverished environments are associated with a very large diversity of species and an equally large array of mechanisms to enhance P-acquisition and P-conservation. Although this was already known, the relationships between these traits and the variation across different locations have not been further explored. The main conclusions of this thesis (chapter 5) include the discovery of specialised root structures in Brazilian rupestrian field specimens, including cluster roots in Proteaceae, cluster-like roots in Cactaceae and Cyperaceae, and sand-binding roots in Eriocaulaceae. The field work in Brazil also allowed us to discover a new species of Xyridaceae, and to conclude that the rupestrian fields are functionally equivalent to the fymbos and kwongan in terms of phosphorus nutrition. It made apparent how much there is yet to be learned from the vulnerable and diverse ecosystem that is the rupestrian fields. From one glasshouse experiment, I was also able to conclude that cluster root formation was positively correlated to mycorrhizal colonization in Viminaria juncea, which is a species that was able to maintain stable shoot phosphorus concentration across a wide range of treatments (0-50 mg P kg-1 dry soil). Probably due to the internal regulation of P, V. juncea did not supress the mycorrhizal colonization or the cluster root formation even at the highest treatments. An additional glasshouse experiment with four Australian native species provided us with an inverse correlation between P-uptake down-regulation and P resorption from senescing leaves. This means that the species which were able to remobilise P from senescing leaves more efficiently were less able to down-regulate their P-uptake, and ultimately suffered from P toxicity. I believe that a broader, more generalised understanding of plant nutrition arises from studies where the interactions between characteristics are explored, and where different areas or different species are studied comparatively; this is what I aimed to achieve in 7 this thesis. The work I present in this thesis is important because it inter-connects knowledge of plant ecophysiology while adding new information and discussion; it has the practical application of being useful in the conservation and revegetation of the kwongan, fynbos and rupestrian fields, which are biodiversity hotspots; and finally, it adds to the early stages of the path of crop species manipulation for increased P-uptake and P-conservation which could result in less fertiliser use and decreased environmental damages from nutrient leaching into water bodies. 8 Statement of original contribution The research presented in this thesis is an original contribution to the field of Plant Ecophysiology. The hypotheses and experiments presented and discussed in this thesis are my own original ideas and writing. People who have made important contributions to this research in addition to those acknowledged in chapters 2, 3 and 4 are: Hans Lambers, Stuart James Pearse and Rafael Silva Oliveira, who were the supervisors of my doctorate and who have guided me through the processes of forming hypotheses, designing experiments and writing the manuscripts. Ricardo Brancalion, who provided technical support with ICP-OES analysis of leaf material included in chapter 2. Michael Smirk, who provided technical support with ICP-OES analysis of leaf material included in chapters 3 and 4. This thesis has been completed during the course of enrolment in a PhD degree at the University of Western Australia, and has not been previously used for a degree or diploma at any other institution.
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