Elizabeth Waters

Associate Professor
Department of Biology
San Diego State University
Evolutionary Biology (EB) program area

Ph.D., Washington University (1993)

Email: ewaters"at"mail.sdsu.edu


Evolution of Protein Families and the evolution of the heat shock response:
The focus of my work has been the evolution of protein families and the evolution of thermotolerance. I have taken a number of approaches in my work including the analysis of gene and protein variation within and between species, comparative molecular biology, and comparative genomics including transcriptome analysis.

A.   The evolution of the heat shock protein families in algae and land plants.



from Rensing et al 2008

What is heat shock? All organisms have a heat shock response and use it to respond to high temperature and other environmental stresses.  During heat shock HSPs (heat shock proteins) are produced (including the HSP100, 90, 70, 60 and small HSP families). All organisms can withstand changes in ambient temperatures. However, the sessile nature of plants, makes tolerance to temperature extremes a necessity for the completion of the life cycle. 

Heat Shock and the Land Plants: The transition from life in the water to life on land required tolerance to more rapid changes in temperatures and to desiccation conditions. Many aspects of the heat shock response are highly conserved across all organisms; however, there are some notable differences between the heat shock response of plants and that of other organisms (Waters and Vierling, 1999a, 1999b). In plants the small HSPs (sHSPs) are a particularly important component of the heat shock response, making up the bulk of the protein produced during heat shock.  These proteins have been shown to be molecular chaperones (that is they assist in the folding of other proteins and can prevent irreversible denaturation of proteins). Compared to the sHSPs of other organisms, the plant sHSPs are also unusually diverse as well as numerous.  Angiosperm species have as many as 40 different sHSPs, individual plant sHSPs have been found to localize to numerous cell compartments including the peroxisome, ER system, mitochondria, chloroplast, as well as to the cytosol (Waters, 1995; Waters et al 2008). The number, diversity and evolutionary history of the plant sHSPs suggest that these protein families diversified within the plant lineage and have evolved plant-specific functions. I am interested in the timing of the diversification of the heat shock protein families and the relationship of this to major events in organsismal evolution such as the origin of land plants.

My recent work includes the comparative genome analysis of a number of complete algal genomes as well as the genome of Physcomitrella patens (Rensing et al 2008). We have found that the green algae do not share the diversity of sHSPs (Waters and Rioflorido 2007) seen in land plants.  In addition, mosses share with vascular plants a diversity of cytosolic HSP70s (Renner and Waters 2007) not found in algae.  My lab has also shown that while all organisms have sHSPs, only land plants have distinct organelle-localized sHSPs families (Waters and Vierling, 1999a, 1999b, Waters and Rioflorido 2007; Waters et al 2008a). Among the sHSP families I have looked specifically at the evolution of the Chloroplast or CP localized family (Waters and Vierling 1999b; Waters and Rioflorido 2007; Waters et al 2008a). It has been well established that the CP sHSPs have a highly conserved methionine-rich region that forms an amphipathic alpha-helix. The methionine residues are completely conserved across angiosperms. These conserved residues have been the subject of much speculation as to their importance in CP sHSP function. I have shown that while a moss (F. hygrometrica) has CP sHSPs, the methionine residues are not present (Waters and Vierling 1999b). I hypothesized that there was a transition in the function of the CP sHSPs (and thus selective constraint acting on this protein) during plant evolution. The National Science Foundation has supported my research on the evolution of the heat shock proteins in algae and land plants.        

B. Positive natural selection is driving the evolution of the HSP70s in Diguetid spiders.   

Diguetia canities male (by J. Starrett)

 To understand how organisms can attain thermotolerance my lab has examined organisms that inhabit the deserts of the American Southwest with close relatives that are restricted to cooler coastal or mountain regions. My former MS student Jim Starrett has found that compared to their close relatives found in temperate areas (the Pholcids and Plecuturids) the Diguetia spiders, which are desert living, have novel HSP70 proteins (Starrett and Waters 2007). This work was the first demonstration that positive natural selection has been acting on these normally highly conserved proteins and our findings challenges some previous assumptions concerning how the HSPs evolve and the possible mechanisms of organismal thermotolerance.

C. Evolution of thermal tolerance in Arabidopsis thaliana and Boechera: Transcriptomics and Gene Evolution

With my collaborator Joan Chen at SDSU my lab has been working on a project on the evolution of the heat shock proteins in Arabidopsis thaliana. A. thaliana has a very wide distribution, from northern Russia, Finland and Sweden to Asia and Africa, this suggest that this species has adapted to an equally wide range of environmental conditions and stresses.

Recently, I have begun a population genetic study of two families of heat shock proteins (HSP100 and the sHSPs) among a number of A. thaliana populations from different environments (e.g. Russia, Italy, Nepal, Morocco, Sweden) (Waters et al 2008b).  My lab has also been examining the gene expression changes in Arabidopsis during both cold and heat stress.  We have found considerable differences among Arabidopsis populations in their responses to stress.  This research has been supported by grants from the California State Program in Research and Education in Biotechnology.

The evolution of thermotolerance in the California Boechera.

Boechera pulchra by L. Ortmann

I have a current National Science Foundation grant to fund research on the evolution of the heat shock proteins and the heat shock response in four species of Rockcress plants (Brassicaceae family, Boechera genus). These plants are native to California. Two of these species live in deserts and two are found either on the coast or in the mountains. These plants differ in their ability to survive and grow when exposed to high temperatures. Plants cannot move away or avoid high temperature stress and therefore, the ability to survive high temperature stress is a very important trait for plants. While heat stress has been studied in some crop species very little is known of the differences in tolerance to stress among wild plant species. This project will address this important but yet under studied question. In order to obtain a full understanding of how Rockcress plants respond to high temperature stress studies will be conducted that will examine rates of photosynthesis, and overall plant growth. In addition, the gene expression patterns of both the heat-tolerant and heat-sensitive plants will be examined both before and after stress. By examining the patterns of gene expression among species that respond differently to stress the researchers will identify novel genes and proteins that provide tolerance to heat stress. We will examine the transcriptome of these species using deep sequencing.  In addition to deepening our understanding of how wild plants adapt to stress this research will also provide information that will assist in understanding how crop species may acquire tolerance to heat stress.


Elizabeth Waters
Department of Biology
San Diego State University
San Diego, CA 92182-4614
fax: 619-594-5676
Office: LS 208B
Lab: LS 208