Author ORCID Identifier

https://orcid.org/0000-0002-7727-2616

Date Available

4-28-2023

Year of Publication

2023

Degree Name

Doctor of Philosophy (PhD)

Document Type

Doctoral Dissertation

College

Agriculture, Food and Environment

Department/School/Program

Plant and Soil Sciences

First Advisor

Dr. Carlos M. Rodríguez López

Abstract

Plants adapt to extreme environmental conditions through physiological adaptations, which are usually transient. Recent research has suggested that environmental conditions can activate a memory of stress that can result in a primed response to subsequent stress events. While the effect of priming has been observed in many plants, the underlying mechanisms are puzzling and seldom studied. A large body of research has been developed in the last decade linking response to stress, stress priming, and memory of stress with epigenetic mechanisms. This understanding of plant epigenetics has opened the door to the application of epigenetics to crop improvement, such as the use of epigenetic breeding for the generation of more resilient crops. Although well-studied in annual and model species, research on epigenetic memory of stress in perennials is still minimal. Viticulture, a perennial form of agriculture, is highly dependent on climatic conditions, not only for yield but also for fruit quality, which is the most important factor affecting produce value at the farm gate and would benefit from more in-depth knowledge on epigenetic memory of stress.

Here we present the results of an experiment conducted over two growing seasons, which constitute the first comprehensive study providing insights into the memory of stress establishment and temporal maintenance, and its potential effect on priming in a perennial crop. Gene expression and DNA methylation data were obtained from 222 plants exposed to the most common forms of abiotic stress faced by vineyards (drought, heat, and combined drought and heat). Our results indicate that the effect of the combined stress on physiology and gene expression is more severe than that of individual stresses, but not simply additive. Common genes expressed under both individual and combined treatments included heat-shock proteins, mitogen-activated kinases, and sugar-metabolizing enzymes, while phenylpropanoid biosynthesis and histone-modifying genes were unique to the combined stress treatment. We also found evidence of the establishment of memory of stress after the heat and combined stress, but not after drought, and that epigenetic chromatin modifications may play an important role during this process. Additionally, we identified genes that are differentially expressed in primed plants one year after their initial exposure to environmental insult and in the absence of recurrent stress. Moreover, primed plants showed a stronger response in gene expression to recurrent stress than plants exposed for the first time to that same stress.

Finally, we explored the effect that two types of vegetative propagation may have on the maintenance of epigenetic memory of stress in primed grapevines. Briefly, although primed propagules generated using callused cuttings presented more differentially expressed genes in response to a second stress than those propagated using layering, only primed layered propagules showed differentially expressed genes in the absence of a recurrent stress, suggesting that the established stress memory is, at least partially, lost during cutting propagation.

Collectively, our results constitute the first molecular evidence of long-term stress memory in grapevine and lay the foundation for the development of a comprehensive model integrating plant response to stress, the establishment of epigenetic memory of stress, and its maintenance, over time and during vegetative propagation in perennial plants.

Digital Object Identifier (DOI)

https://doi.org/10.13023/etd.2023.111

Supplemental File S1.zip (24851 kB)
Supplemental Figures and Tables for Chapter 2

Supplemental File S2.zip (1633 kB)
Supplemental Figures and Tables for Chapter 3

Supplemental File S3.zip (1338 kB)
Supplemental Figures and Tables for Chapter 4

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