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Physiological and Molecular Basis of Salt and Waterlogging

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Comparative molecular physiology of salt and waterlogging tolerance in Lotus tenuis and L. corniculatus: towards a perennial pasture legume for saline land Natasha Lea Teakle This thesis is presented for the degree of Doctor of Philosophy The University of Western Australia School of Plant Biology Faculty of Natural and Agricultural Sciences June 2008 ABSTRACT Salinity and waterlogging interact to reduce the growth of most crop and pasture species. Species that are productive on saline-waterlogging land are needed for Australian farming systems. One option is Lotus tenuis, a perennial legume widely grown for pasture in the flood-prone and salt-affected Pampa region of Argentina. To identify mechanisms responsible for the adverse interaction between salinity and waterlogging, Lotus tenuis with a reputation for tolerance was compared with L. corniculatus, the most widely cultivated Lotus species. The physiology of salt and waterlogging tolerance in L. tenuis (4 cultivars) was evaluated, and compared with L. corniculatus (3 cultivars). Overall, L. tenuis cultivars accumulated less Na+ and Cl-, and more K+ in shoots than L. corniculatus cultivars, when exposed to 200 mM NaCl for 28 d in aerated or in anoxic (stagnant agar) solutions. In a NaCl dose response experiment (0 to 400 mM NaCl in aerated solution), Lotus tenuis (cv. Chaja) accumulated half as much Cl- in its shoots than L. corniculatus (cv. San Gabriel) at all external NaCl concentrations, and about 30% less shoot Na+ in treatments above 250 mM NaCl. Ion distributions in shoots were determined for plants at 200 mM NaCl; L. tenuis (cv. Chaja) accumulated about half as much Cl- in old leaves, young leaves and stems, compared with concentrations in L. corniculatus (cv. San Gabriel). There were not, however, significant differences between the two species for Na+ concentrations in the various shoot tissues under aerated NaCl treatment. To determine the cause of the differences in shoot concentrations between the Lotus species, xylem concentrations of Na+ and Cl- were measured in sap collected using spittlebugs (Philaenus spumarius) from plants in saline (200 mM NaCl) and/or stagnant treatments over 4 weeks. In aerated-NaCl solution (200 mM), L. corniculatus had 50% higher Cl- concentrations in the xylem and shoot compared with L. tenuis, whereas concentrations of neither Na+ nor K+ differed between the species after 28 d treatment. In stagnant-plus-NaCl solution, xylem Cl- and Na+ concentrations of L. corniculatus increased to twice those of L. tenuis. These differences in xylem ion concentrations, which were not caused by variation in transpiration between the two species, contributed to lower net accumulation of Na+ and Cl- in shoots of L. tenuis, indicating ion transport mechanisms in roots of L. tenuis were contributing to better ‘exclusion’ of Cl- and Na+ from shoots, compared with L. corniculatus. Thus, Cl- ‘exclusion’ is a key trait contributing to salt tolerance of L. tenuis; and ‘exclusion’ of both Cl- and Na+ from the xylem enables L. tenuis to better tolerate the interactive stresses of salinity and waterlogging. Enhanced root aeration would contribute to maintaining Na+ and Cl- transport processes in roots of plants exposed to stagnant-plus-NaCl treatments. Measurements of radial O2 loss (ROL) under stagnant conditions indicated that L. tenuis roots exhibit a partial barrier to ROL and had higher O2 concentrations at root tips, compared with L. corniculatus. Root porosity was also higher in L. tenuis, due to constitutive aerenchyma. Therefore, enhanced root aeration might have contributed to the maintenance of Na+ and Cl- ‘exclusion’ in roots of L. tenuis exposed to the stagnant-plus-NaCl treatments. Lotus tenuis also had greater dry mass than L. corniculatus after 56 d in NaCl or stagnant-plus-NaCl treatment, demonstrating greater tolerance to these stresses over time. To further understand the mechanisms of Cl- transport under salt stress, 36Cl tracer experiments were conducted at steady-state Cl- uptake after 4 d treatment at 200 mM NaCl. The two species did not differ in unidirectional uptake of Cl-, but rather transport of Cl- from roots to shoots started sooner in L. corniculatus and was twice the rate of L. tenuis under saline treatment. In addition, L. tenuis has greater efflux of Cl-, and thus maintains lower total Cl- concentrations over time. A possible candidate gene involved in regulation of Cl- transport in L. tenuis could be a cation-chloride cotransporter (CCC). CCCs are predicted to play a role in salt tolerance of plants, particularly when Na+ and Cl- are co-transported across membranes. A CCC gene was cloned from L. tenuis (LtCCC); protein sequence analysis showed LtCCC had 80% homology to an Arabidopsis CCC, and 91% with a putative Medicago truncatula CCC. Results from real-time qPCR showed expression of LtCCC increased under salt stress for L. tenuis roots, but not in L. corniculatus. Therefore, LtCCC may contribute to the control of root-to-shoot Cl- transport, and therefore differences in salt tolerance between L. tenuis and L. corniculatus. The combination of salinity and anoxic stress leads to differences in Na+ transport, in addition to Cl-, between L. tenuis and L. corniculatus. At the root level, L. tenuis had 17% higher root and 25% lower shoot Na+ concentration than L. corniculatus after 9 d stagnant-plus-NaCl treatment. Therefore, during early stages of exposure to salinity, L. tenuis accumulated a higher proportion of total Na+ in the roots under combined stagnant-plus-NaCl treatment (55% versus 39% for L. corniculatus). Na+ transporters, particularly those relying on H+ gradients across membranes, which in turn require adequate ATP levels, could be impaired under O2 deficits that inhibit respiration. To + study the effect of O2 deficiency on a Na transporter, an NHX1-like gene was cloned from L. tenuis and identity established via sequencing and yeast complementation studies. Real-time qPCR showed expression of NHX1 in L. tenuis roots increased under stagnant-plus-NaCl treatment, whereas it was reduced in L. corniculatus. Thus, maintaining O2 transport to roots, together with up-regulation of an NHX1-like gene for Na+ accumulation in vacuoles, contributes to tolerance of L. tenuis to combined salinity and waterlogging stresses. This study highlights the importance of minimising Cl- transport to shoots as a mechanism of salt tolerance and has identified a CCC-like gene in L. tenuis as a candidate for mediating root-to-shoot Cl- transport. Under combined stagnant-plus-NaCl treatment, control of Na+ transport is another mechanism contributing to tolerance in these Lotus species. Enhanced root aeration in L. tenuis maintains root Na+ transport processes, such as accumulation in vacuoles via NHX1-like genes, to diminish xylem loading to the shoot. Overall, this thesis has contributed new knowledge on the potential of Lotus tenuis as a saltland pasture and has significantly enhanced current understanding on the mechanisms of salinity and waterlogging tolerance in plants. ACKNOWLEDGEMENTS Firstly, I would like to thank my supervisors Tim Colmer and Daniel Real. Thank you for encouraging and motivating me during the last few years. No matter how busy, you always found time to discuss protocols, read drafts, listen to my complaints about failed experiments and ‘de-stress’ me! You have also assisted greatly in my career development by helping create new contacts, encouraging me to go overseas for extended research trips and assisting with applications. The enthusiasm, attention to detail and work ethic you both display inspires me to strive for excellence in my own work. I am grateful to the Grains Research and Development Corporation for my PhD Scholarship and the AW Howard fund for a top-up stipend. Special thanks also to the Salinity CRC for extra research funds and professional development. The overseas research would not have been possible without the financial support of the AW Howard travel awards, Mary Janet Lindsay of Yanchep Memorial fund and the UWA travel award. Thanks to Anna Amtmann for letting me complete 12 months research towards my thesis at Glasgow University, UK. I loved my time in Scotland and the Amtmann/Blatt group was fantastic to work with. Special thanks to Annegret, for assisting with toad operations, and surviving with me the frustrating months of dying oocytes! Thanks also to Bernie, Patrick, Richard and Bo for all your advice. Special thanks to Tim Flowers for letting me complete 3 months research at Sussex University, UK, and most importantly for introducing me to the wonderful spittlebugs! I am very appreciative of how welcoming you and your family were to me during my time in Sussex. Thanks to the members of the Plant Ecophysiology group at UWA (‘Colmerites’!), both past (Jeremy, Imran, Kirsten) and present members (there are now too many to name!) who assisted me greatly in preparing for experiments and harvests. Thanks to Hans and the office staff for assisting with the administrative requirements of my PhD. I also received fantastic assistance from Gary, Elizabeth and Hai (student labs), Leon and staff (glasshouses) and Alan and Sean (computing). Special thanks to my family for their support during the last few years and putting up with me being a ‘poor student’ for so long. Having a family of farmers helped me always keep the science in perspective. Finally, and most importantly, my heart-felt thanks to ‘Sir’ James, the world’s greatest pot lid alfoiler! You put up with the crazy hours I worked
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