Multiplicity in Unity: Plant Subindividual Variation and Interactions with Animals

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American Journal of Botany 92, Maternal provisioning, sibling rivalry and seed mass variability in the dioecious shurb Rhamnus alpinus. Evolutionary Ecology 17, Seed mass effects on performance of Pinus halepensis Mill. Forest Ecology and Management , Castellanos M. Subindividual variation and genetic versus environmental effects on seed traits in a European Aquilegia.

Botany 86, Castro J. Seed mass versus seedling performance in Scots pine: a maternally dependent trait. New Phytologist , Short delay in timing of emergence determines establishment success in Pinus sylvestris across microhabitats. Annals of Botany 98, Seedling establishment of a boreal tree species Pinus sylvestris at its southernbmost distribution limit: consequences of being in a marginal Mediterranean habitat.

Journal of Ecology 92, Seed size. In: Handbook of seed science and technology. Evidence that the negative relationship between seed mass and relative growth rate is not physiological but linked to species identity: a within-family analysis of Scots pine.

Tree physiology 28, Mechanisms blocking Pinus sylvestris colonization of Mediterranean mountain meadows. Journal of Vegetation Science 13, Crean A. Coping with environmental uncertainty: dynamic bet hedging as a maternal effect.

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Phil Trans R Soc B , Creus J. Montes 54, Debain S. Seed mass, seed dispersal capacity, and seedling performance in a Pinus sylvestris population. Ecoscience 10, Cone and seed trait variation in whitebark pine Pinus albicaulis; Pinaceae and the potential for phenotypic selection. American Journal of Botany 96, Bigger is not always better: conflicting selective pressures on seed size in Quercus ilex. Evolution 58, Halpern S. Sources and consequences of seed size variation in Lupinus perennis Fabaceae : adaptive and non-adaptive hypotheses.

Herrera C. Multiplicity in unity. Plant subindividual variation and interactions with animals. The University of Chicago Press.

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Pine processionary caterpillar Thaumetopoea pityocampa as a new threat for relict Mediterranean Scots pine forests under climatic warming. Biological Conservation , Users without a subscription are not able to see the full content. Herrera Abstract The main purpose of this book is to present the message that when one looks at subindividual variability, a feature that was either unnoticed or taken as a nuisance turns into an opportunity for framing new questions, identifying novel biological mechanisms linking sessile plants and mobile choosy animals, and deepening the understanding of the ecological and evolutionary factors involved in plant—animal interactions.

More The main purpose of this book is to present the message that when one looks at subindividual variability, a feature that was either unnoticed or taken as a nuisance turns into an opportunity for framing new questions, identifying novel biological mechanisms linking sessile plants and mobile choosy animals, and deepening the understanding of the ecological and evolutionary factors involved in plant—animal interactions. Authors Affiliations are at time of print publication. Carlos M. Herrera, author More Less. Print Save Cite Email Share. Show Summary Details. Subscriber Login Email Address.

Library Card. View: no detail some detail full detail. Front Matter Title Pages Preface. Chapter One Introduction. Hence intraorganismal selection could be a way for them to circumvent this limitation Clarke The genetic mosaic [6] theory of plant defense Whitham and Slobodchikoff ; Gill et al. Published studies aiming to evaluate the importance of intra-individual genetic variability in plants are scarce, and this is not just a recent trend Sutherland and Watkinson ; Herrera In addition, it has been difficult to prove that such variations have been sources of clear gains in fitness for plants, and that intra-individual variations provide protection against predators Buss They cite papers showing variations in a fig tree used for bonsai, in juniper, tobacco, pelargonium, and maize.

Except in two studies dedicated to mangrove trees and fig trees from Panama, all these species are intensively manipulated for and by humans. Published examples of mosaicism observed in plants include a single eucalyptus tree showing variation for volatile oil composition Edwards et al.

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It is one of the very few genetic mosaics that have been described among non-clonal plants and non-crop species Padovan et al. In the morning glory Ipomoea , somatic mutations caused by the excision of a transposon create heritable flower color variations Inagaki et al.

The flower color phenotypes are thought to have been selected by pre-Columbian peoples who favored plants answering in more flexible ways to their domestication wishes Glover et al. In a thorough review, Herrera observes that descriptions of genetic mosaicism among cultivated plants are abundant, while there is very little evidence gathered from wild plants, and that evidence is mostly gathered in an indirect way. Noticing the extreme scarcity of unambiguous cases of genetic mosaics in wild plants, despite biased research efforts toward species expected to be more prone to mosaics long-lived, clonal, highly branched , Herrera hypothesizes that they are far less frequent among wild plants than among cultivated plants Herrera Domesticated peach, compared to wild peach, did not show any increase in recombination rate and mutation rate near recombination events in a sequencing study Wang et al.

However, no general conclusion can be derived from this unique study with its sample size of one.


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In common bean, for instance, domestication has a pervasive effect throughout the genome for both gene expression patterns and diversity, and it is responsible for an overall reduction in diversity associated with an increase in the functional diversity at target loci Belluci et al.

The genetic diversity of cultivated species, engineered by human agency, is indeed particular Gerber The place of domesticated plants in the debate about plant individuality must therefore be questioned. If, as Hull said, vertebrates bias the way biological individuality is understood, cultivated plants might similarly bias the way plant individual heterogeneity is understood, and thus our understanding of plant individuality as a whole.

When data are available, comparison of assertions made about particular plant species with information provided by genetic diversity analyses of the same species can be enlightening. The genetic diversity of Pando, our large aspen clone, was studied with microsatellite markers, and Mock et al. In a broader zone, a large number of different genotypes was revealed. The hypothesis of a predominantly clonal evolution of the population did not fit with the observations. The few papers dealing with plants in philosophy of biology often refer to the Pando case.

If clonality is indeed important in Pando, sexual reproduction is present, providing genetic novelty. Moreover, the clone is much more recent than previously assumed, and somatic mutations, supposed to play a major role in the clone functioning, are not that important. Trends similar to Pando were observed in other Populus species in Spain, in a hybrid Populus alba - Populus tremula clonal zone Macaya-Sanz et al.

Our apomictic Taraxacum species, dandelion, highlighted by Janzen , has also been studied with molecular tools. Genetic mutations were detected between generations, at a low rate, in the absence of sexual reproduction—that is, without meiosis King and Schaal In the same species, different stresses were similarly shown to trigger considerable DNA methylation variation throughout the genome, and that was inherited through successive generations, highlighting the potential of epigenetic inheritance in evolutionary processes Verhoeven et al.

One of the oldest domesticated species, grapevine, is particularly well studied with the tools of molecular biology. Sexual reproduction remained important in the history of vine domestication, as can be observed in pedigree reconstruction; for instance, Chardonnay resulted from a cross between Pinot and Gouais blanc Bowers et al. They might play an important role in plant evolution, in cultivated as well as wild plants, and could partly explain the peculiarities of this kingdom Biemont and Vieira Among other traits, berry skin color, probably dark at the origin, was turned light by transposition and maintained by domestication.

The cluster size and shape of the cultivar Carignan were modified by transposon activity This et al. Sexual reproduction, with recombinations, provides one of the mechanisms suppressing mobile elements. On the opposite side, long term vegetative propagation—associated with aggressive management toward plants to increase productivity grafting, pruning, etc. Rice domestication displays the same trend Naito et al. The phenotype of an organism can be modified by some epigenetic [7] information, that can be conserved and inherited in a stable way. Examples are described in wild and cultivated plants Jablonka and Raz : the symmetry of the Linaria vulgaris flower is modified by a methylation that is heritable Cubas et al.

DNA modification through cytosine methylation, related to transposable elements Law and Jacobsen , is one of the mechanisms that can produce epialleles stably transmitted during meioses, having transcription effects and therefore consequences for morphology. Overall, the detailed genetic analyses of some plant species from our herbiary provide contrasting visions of plant diversity.

On the one hand, clonality is indeed important in aspen, but sexual reproduction, which supplies genetic novelty, is still there, and the clone, which is much more recent than assumed, exhibits few somatic mutations. Similarly, dandelion possesses sexual reproduction that has been underestimated and exhibits epigenetic variations.

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Grapevine genetic diversity has been determined by viticultural practices that favored the emergence of phenotypic novelties and their maintenance , mostly through somatic mutations and the spread of transposons. We see here that human management of plants and their domestication have consequences for the generation of diversity and for its conservation. Molecular stories of the herbiary are rich and sometimes reveal phenomena that were not previously foreseen.

Following insights into the complexity of plant genome, we must come back to the whole plant.

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If the architectural models from botanists described above, used to analyze plant growth, were extended to a genetic dimension, a single tree could be made of a population of genotypes. He launched experiments to study the possible genetic heterogeneity of at least six single tropical trees with genetic markers—two species in Guyana , one species in Gabon , and three species in Madagascar Chevallier, C.

Lanaud, personal communications, Population geneticists working on forest trees usually wild but also planted species will probably not be surprised by these unpublished results. Indeed, in their studies, population geneticists sample various kinds of material leaf, phloem, cambium, and bud from any part of a tree to obtain its genotype. The observed intra-tree heterogeneity remains low, with a rate of the same order of magnitude as genotyping error. The consistency of a single tree genotypic information makes it possible, for instance, to reconstruct relatedness and perform successful parentage analyses Gerber et al.

The assumption made by Whitham and Slobodchikoff can therefore be questioned. This hypothesis of a loss of parental genotypes, illustrated with a cultivated plant example and cited by Clarke , does not correspond to the everyday experiments of tree population geneticists, who observe consistent genetic data over the space of tree organisms and their generation time. The Pando genetic analysis is in accordance with these experiments, suggesting a minor importance for somatic mutations, far from the one previously assumed. The rate of molecular evolution is driven by generation time; it is low in trees and shrubs, which have long generation times, as compared with herbaceous plants, which have shorter generation times Smith and Donoghue Families of taller plants are characterized by lower mutation rates per unit of time in nuclear, chloroplast, and mitochondrial genomes Lanfear et al.

Moreover, somatic mutations accumulate during plant aging Dubrovina and Kiselev Accordingly, in testing on compiled data species the possible difference between within-plant phenotypic variability of small, short-lived plants, in comparison with large, long-lived plants, no greater subindividual variability among comparatively larger and longer-lived plants was observed Herrera Using cell-lineage analysis and modeling, Burian et al. Surprisingly, the plant is also setting aside a quiescent population of cells for gamete production Groot and Laux Burian et al.

Contradicting the commonplace idea of highly heterogeneous plants, and especially trees, these mechanisms extend plant lifespan, a result also shown by Watson et al. The demonstration of the presence of a slowly dividing functional germline in most plant species is about to bring them much closer to animal functioning Lanfear Nevertheless, estimation of the existence and the importance of intra-individual diversity in trees and plants remains to be done, by assessing and comparing variability at the different genome layers with -ome suffixed names: genome, transcriptome, proteome, methylome, epigenome, mobilome, etc.

This will help us understand the levels of diversity, their origins, their phenotypic effects, and their evolutionary importance. The analysis of genome-wide changes due to crop domestication and breeding is now reachable Shi and Lai Genotyping errors are of course always present, due to mistakes that can take place at any step of experiments, from sampling errors to molecular biology reaction problems, to miscoding of samples or data, to error in analyses, and others.

Multiplicity in Unity

Genotyping errors can also be confused with true mutations, somatic mutation frequency probably being lower than mistyping rate. But there is no reason why those errors should be more numerous in plant studies than in animal studies. Several studies have aimed to analyze within-plant genetic heterogeneity. Results are often unclear, or unpublished, or support limited possible generalizations.

In a short news publication, Yong described the genome-wide sequence analysis of several samples of black cottonwood trees Populus trichocarpa , with reference to its genome, which was fully sequenced in Olds, personal communication, Several steps are involved in this technique that probably generate uncertainty and inaccuracy, many replicates should have been done, and sample variation should have been given. The results thus appear unreliable. We have identified at least three studies aimed at evaluating the DNA variability inside a single pedunculate oak tree Quercus robur based on recent sequencing technologies.

The first project was presented in [8] and considered a year-old tree. Four leaves from three branches were compared by high throughput sequencing, and almost point mutations were identified between branches M. Blaxter, personal communication, No published results are available. The second project Napoleome aimed at sequencing the genome of two leaf samples collected at the top and bottom branches of a single year-old oak tree on the Lausanne University campus. A low number of somatic mutations was detected Schmid-Siegert et al.

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