Desiccation Sensitive Seeds: Understanding Their Evolution, Genetics and Physiology
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Desiccation sensitive seeds: Understanding their evolution, genetics and physiology Alexandre Correia Silva de Santana Marques Thesis committee Promotor Prof. Dr Richard G.H. Immink Special professor Physiology of Flower Bulbs Wageningen University & Research Co-promotors Dr Henk W.M. Hilhorst Associate professor, Laboratory of Plant Physiology Wageningen University & Research Dr Wilco Ligterink Assistant professor, Laboratory of Plant Physiology Wageningen University & Research Other members Prof. Dr Bas J. Zwaan, Wageningen University & Research Dr Koen Verhoeven, Netherlands Institute of Ecology (NIOO-KNAW), Wageningen Dr Peter E. Toorop, Monsanto Vegetable Seeds Division, Bergschenhoek Dr Wouter Kohlen, Wageningen University & Research This research was conducted under the auspices of the Graduate School Experimental Plant Science Desiccation sensitive seeds: Understanding their evolution, genetics and physiology Alexandre Correia Silva de Santana Marques Thesis submitted in fulfilment of the requirements for the degree of doctor at Wageningen University by the authority of the Rector Magnificus, Prof. Dr A.P.J. Mol, in the presence of the Thesis Committee appointed by the Academic Board to be defended in public on Tuesday 22 May 2018 at 11 a.m. in the Aula. Alexandre Correia Silva de Santana Marques Desiccation sensitive seeds: Understanding their evolution, genetics and physiology, 189 pages PhD thesis, Wageningen University, Wageningen, the Netherlands (2018) With references, with summary in English ISBN 978-94-6343-859-9 DOI https://doi.org/10.18174/446523 Preface In tropical rainforests we can find a huge diversity of fruits hanging from the trees. Mango, lychee, cacao, avocado, rambutan, mangosteen, jackfruit, coconut, citrus, inga, durian, iamb, and nectandra are just a few examples. Humanity seems not to notice that these forests are shrinking daily. For example, there is only 5% left of the original Brazilian Atlantic forest. The Amazon forest is still there because it is more isolated, but it has been severely deforested and 80% of its original vegetation is left. The main cause of deforestation is farming, by which forest is replaced by grass fields. This consumes huge areas of land. I hope that the technologies we are currently developing will change the system of food production soon and bring a halt to deforestation. What can be done after deforestation? Re-forestation. There are seeds stored in seed banks. We can simply grow various plant species back. However, almost up to 50% of the tree species in tropical rain forest develop desiccation sensitive and therefore non- storable seeds. Without an effective method for storing these seeds, we will lose much of plant biodiversity. In the worst case scenario, we and next generations will lose for example, the possibility of eating the fruits I cited above, because these plants produce all non-storable seeds. We must investigate this problem, to understand the physiology and genetics of these plants in order to support the development of methods to overcome these storability issue. The work described in this PhD thesis is a step towards the understanding of the seed desiccation sensitivity phenomenon. I sincerely hope that I managed to raise your attention for the beauty, richness and fragility of plant biodiversity on our planet. Please, let’s all do our best to protect biodiversity! “When the last tree is cut down, the last fish eaten, and the last stream poisoned, you will realize that you cannot eat money” (Cree Indian proverb). Contents Chapter 1. General Introduction................................................................................11 Chapter 2. Evolutionary ecophysiology of seed desiccation sensitivity ...............25 Chapter 3. Understanding seed desiccation tolerance by studying seeds of the desiccation sensitive Arabidopsis thaliana abi3-6 mutant......................55 Chapter 4. The ‘recalcitrant’ genome of Castanospermum australe........................93 Chapter 5. Induction of desiccation tolerance in recalcitrant Citrus limon seeds ..139 Chapter 6. General Discussion................................................................................167 Summary....................................................................................................................181 Aknowledgment.........................................................................................................183 Curriculum vitae.......................................................................................................185 Education Statement................................................................................................187 General introduction Seeds are time traveling capsules Time travel is a fascinating quest explored by many sci-fi writers. There is an itchy desire in each of us to discover what will happen in the future. Gipe et al. (1985) invested in physics to develop a machine capable to distort time and take us “back to the future”, although without concrete success till the present time. Other strategies have been conjured up much earlier, consisting e.g. of maintaining the human body desiccated by mummification. This strategy is still not successful in calling dead bodies to life, but freezing approaches are under investigation (Merkle, 1992). Although freezing and calling to life of complete human bodies is still not feasible, freezing cells like spermatozoids, ovules and embryos are medical routines. Thus, time travel is already possible for humans, at least from a solely biological point of view. Similar to freezing and capturing vital cells, many organisms travel through time using their own strategies. Desiccation tolerance1 of plant seeds is one of these strategies, which consists of the capacity of seeds to survive extreme water losses (below 10% of the fresh weight or 0.1 g H2O/g dry weight). Desiccation tolerance is widespread across the propagules of diverse life forms, e.g. bacteria, fungi, protozoa, animals and plants (Crowe, 2014). It assures that these organisms will flourish as soon as water availability returns. In contrast to desiccation tolerance, dormancy is a genetically programmed mechanism that arrests the development of the propagules even when optimal conditions are present and this is also found in diverse life forms. desiccation tolerance, together with dormancy, aims to guarantee the survival of species by spreading propagules through long periods of time and thus avoiding extinction. Evolutionary history of seed desiccation tolerance and sensitivity Desiccation tolerance capacitated the first land plants to conquer terrestrial habitats and it is largely present in vegetative tissues of basal plants and in desiccation tolerant seeds (also termed ‘orthodox’) of spermatophytes (Black and Pritchard, 2002). The evolution of terrestrial plants is believed to be monophyletic and originating from charophycean algae (Zhong et al., 2015). Desiccation tolerance was already present in these algae and is also believed to be carried from these algae towards the vegetative tissues of 1 One needs to distinguish desiccation from drought. Drought characterizes the lack of moisture in the soil (Iljin, W. (1957) Drought resistance in plants and physiological processes. Annual Review of Plant Physiology, 8, 257- 274. while desiccation denotes the lack of moisture in the organism (Moore, J.P., Vicre-Gibouin, M., Farrant, J.M., Driouich, A. (2008) Adaptations of higher plant cell walls to water loss: drought vs desiccation. Physiol Plant, 134, 237-245.. The lack of available water suspends virtually every metabolic activity in the cells, such as respiration and transcription. Thus, it is also different from dormancy or lethargy that reduces in a wet environment the progress of development or of metabolic activity. 11 bryophytes and pteridophytes and later on confined to the seeds of the spermatophytes (Oliver et al., 2000). The monophyletic origin of desiccation tolerance hypothesis is supported by the fact that the regulation of desiccation tolerance involves the phytohormone abscisic acid (ABA) and the transcription factor ABI3 in vegetative tissues of the moss Physcomitrella patens, just as in seeds of numerous angiosperm plants (Khandelwal et al., 2010). Although desiccation tolerance is present in seeds of 95% of the angiosperms, desiccation sensitivity is present in almost half of those present in tropical rainforests (Tweddle et al., 2003). Among them, there is a broad phenotypical variation that has been categorized in ‘recalcitrant’ and ‘intermediate’ seeds with the latter losing viability at lower water contents than the former (Berjak and Pammenter, 2013). It has been suggested that desiccation sensitive (DS)-seeded species evolved from desiccation tolerant (DT) ones adapting to environments where the conditions were conducive to immediate germination, e.g. tropical rainforests with abundant and constant water regimes. In these environments, desiccation tolerance is not an adaptive trait and it can eventually get lost in these species (Berjak and Pammenter, 2013; Farrant et al., 1993a). Depending on the environment, DS-seeded species may show a gradient of dehydration tolerance. For example, the seeds of Acer pseudoplatanus and Coffea arabica display varying dehydration tolerance levels across their native plant distribution ranges (Daws and Pritchard, 2008; Ellis et al., 1991). The intraspecific variability observed for seed desiccation tolerance reflects the high plasticity of this trait and