The adaptive potential of plant endopolyploidy in response to herbivory

endopolyploidy;Herbivory;Overcompensation;Plant;Endoreduplication;Endocycle;Ploidy;Damage;Herbivore;Arabidopsis

Scholes, Daniel

关键词: endopolyploidy;    Herbivory;    Overcompensation;    Plant;    Endoreduplication;    Endocycle;    Ploidy;    Damage;    Herbivore;    Arabidopsis;   

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美国|英语

来源: The Illinois Digital Environment for Access to Learning and Scholarship

【 摘 要 】

Damage caused by herbivores is a potentially strong selective agent of plant phenotypes, including selecting for many defensive traits, though not all plant-herbivore interactions are strictly negative for the plants.Overcompensation is the increase in components of fitness (flower, fruit, and/or seed yield) following herbivory.Studies by Paige and Whitham (1987) showed that when ungulate herbivores removed 95% or more of the above-ground biomass of the monocarpic biennial scarlet gilia, Ipomopsis aggregata, the product of lifetime seed production, seed germination, and seedling survival averaged 3.0 times that of uneaten controls (see also Paige 1992, 1994, 1999).The increase in relative fitness was largely due to architectural changes in the plant; removal of scarlet gilia’s single inflorescence resulted in the production of multiple flowering stalks due to the release of apical dominance and an overall increase in both above- and below-ground biomass.Given that the release of apical dominance undoubtedly alters both genetic and physiological processes to maximize rapid regrowth (particularly in axillary bud break and stem elongation), recent studies have targeted possible mechanisms for facilitating rapid regrowth in overcompensating organisms.One possible mechanism is the replication of the genome without mitotic cell division via an alternative cell cycle under genetic regulation, termed endoreduplication (Brodsky and Uryvaeva 1977, Nagl 1976).Removal of apical dominance by herbivory reduces the level of auxin in the remaining above-ground tissues and leads to axillary bud break and stem regeneration—high levels of auxin are also known to repress the endocycle, and by contrast, a reduction in levels of auxin triggers an exit from mitotic cycles and an entry into endocycles (Ishida et al. 2010), providing a physiological mechanism for the promotion of endoreduplication following herbivory.While much is known about endoreduplication at the cellular level, little is known regarding the role of endoreduplication in determining organismal fitness, let alone the compensatory response.To investigate the potential role of endoreduplication in fitness compensation following herbivory, two accessions of Arabidopsis thaliana were grown under greenhouse conditions and the bolting inflorescences of half of the plants of each genotype were clipped with scissors, simulating natural herbivory (Chapter 2 of this dissertation).At the induction of senescence, when fitness and endopolyploidy are fully determined, endopolyploidy was measured by flow cytometry on a set of plants from each treatment group.Clipped plants of A. thaliana Columbia, a genotype that historically overcompensates following clipping, displayed greater silique and seed yield than unclipped controls, while clipped plants of A. thaliana Landsberg erecta, a genotype that typically undercompensates, displayed an equal number of siliques but lower total seed yield than unclipped controls.Columbia-4’s overcompensation in fitness measures correlated with an overall increase in nuclear DNA content due to endoreduplication.Landsberg erecta, however, experienced no change in its nuclear DNA content.These results provided the first correlative evidence of endoreduplication’s role in mitigating the stress of herbivory.After the initial discovery of the correlation between endopolyploidy and fitness compensation following herbivory in A. thaliana, I examined the role of endoreduplication as a generalized mitigator of herbivory.To investigate the generality of this relationship, I grew eight recombinant inbred lines produced by a Columbia-4 × Landsberg erecta mating under greenhouse conditions (Chapter 3 of this dissertation).Attributes of fitness and endopolyploidy were measured from clipped and unclipped plants of these eight genotypes and a significant positive relationship between the change in seed yield and the change in endopolyploidy following clipping was observed.This relationship suggests that endopolyploidy and fitness compensation following herbivory are in some way directly linked, since fitness and endopolyploidy are both polygenic traits, and so any chance association between compensation genes and endopolyploidy genes should be broken by recombination upon crossing of the parental genotypes.This result also suggests that the relationship exists for the Columbia family of genotypes generally, since both Columbia-4 and Landsberg erecta originated from the natural Columba population.To further investigate the generality of this relationship, I grew nine globally-distributed natural ecotypes of A. thaliana under greenhouse conditions, encompassing much of its wide geographic range across the Northern Hemisphere (Chapter 3 of this dissertation).Attributes of fitness and endopolyploidy were measured from clipped and unclipped plants of these nine ecotypes.Although no significant relationship was observed between fitness compensation and endopolyploidy following herbivory among these global ecotypes by themselves, little variation in compensation was measured for these ecotypes.The global ecotypes did, however, still fit within the range of values present in the Columbia-family genotypes.To investigate the direct, causal genetic link between the positive relationship observed between endopolyploidy and fitness compensation following herbivory in the Columbia family of genotypes, I grew cell-cycle mutant genotypes to determine if the change in endopolyploidy with the genetic manipulation affected fitness compensation.Specifically, I used T-DNA insertion and CaMV 35S overexpression mutants of INCREASED LEVEL OF POLYPLOIDY1, ILP1, a gene that regulates DNA replication of the endocycle, as well as the Columbia-0 genotype that served as the genetic background for the mutants.The Columbia-0 wildtype displayed decreased seed production, above-ground biomass, and endopolyploidy when clipped relative to when unclipped, providing further evidence of the relationship between endoreduplication and fitness compensation following damage.The two mutant lines, however, did not display changes in any of these measures following clipping damage, possibly due to the loss of natural plasticity in endoreduplication upon ILP1 expression manipulation.Additionally, the ILP1 knockout line, which should have lower endopolyploidy than the Columbia-0 wildtype, actually had greater levels of endopolyploidy, possibly due to an endoreduplication compensatory response induced upon the loss of ILP1 action.Further, the ILP1 overexpression did not have increased levels of endopolyploidy relative to the wildtype as expected.Phosphorus fertilization of these genetic lines improved fitness compensation measures, but only significantly for the Columbia-0 wildtype, further indicating a potential lack of plasticity tied to the experimental gene manipulation.These studies collectively show that fitness compensation following herbivory may be influenced by the organism’s ability to generate endopolyploidy following damage, potentially contributing to regrowth and organismal fitness by increased cell size, increased gene expression, increased water and nutrient transport, and other genetic and/or physiological mechanisms (Lee et al. 2009).While fitness compensation and endopolyploidy have thus far been researched extensively independently, these are the first studies that provide evidence for a relationship between the two phenomena.