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ESSAY |
Biology Department, Davidson College, Box 7118, Davidson, North Carolina 28035-7118
Submitted February 4, 2003; Revised March 17, 2003; Accepted April 1, 2003
| ABSTRACT |
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Key Words: genomic proteomics bioinformatics teaching research undergraduate model organisms online databases public domain
| INTRODUCTION |
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One reason for the increased need to access information is the impact that molecular approaches are having on all areas of biology. Molecular tools have integrated areas within biology previously considered distinct, such as biochemistry, ecology, genetics, and behavior. Biologists working in such different areas within biology now use overlapping information for different applications. With the advent of genomics and its allied fields of proteomics and bioinformatics, integrating information across many subdisciplines of biology is becoming increasingly important for research and teaching. Furthermore, many leaders in genomics, proteomics, and bioinformatics (referred to simply as genomics in this essay) are emphatic about the need to provide free access to data and to electronic research tools. This confluence of needs for information and interdisciplinary learning have led to a unique time in biology education.
Most faculty lack formal training in genomics, but students are eager to learn about genomics and its impact. Faculty are quickly learning to incorporate various aspects of genomics into their curriculum, either by developing new genomics courses or by incorporating bits and pieces of data into existing courses. New editions of textbooks in many areas of biology are including genomic information. However, the field of genomics is more than a compilation of lessons learned. Genomics is a dynamic body of information that can be searched and explored by anyone with Internet access. By accessing online resources, teachers can bring more of the dynamic nature of genomics to students. I have developed a genomics course that I have taught twice (Fall semesters 2001 and 2002; Campbell and Heyer, 2003). This essay outlines some of the online resources my students used to discover genomics by actively exploring freely available research-quality data using bioinformatics tools (Figure 1).
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| TRADITIONS OF INNOVATION |
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Since 1989, Project Kaleidoscope (PKAL; www.pkal.org) has fostered dissemination of teaching innovations that work. Recognizing that science, technology, engineering, and mathematics (STEM) faculty at large and small campuses have made substantial strides in improving education, PKAL has run workshops and written white papers describing what is required to foster change, institutionalize reform, and create educational leaders for the future (PKAL, 2003a). Collaboration is critical to successful education enhancements (PKAL, 2003b). Genomics offers STEM faculty new opportunities to establish collaborations in research and teaching. The integration of research and teaching was recently praised by Tom Cech (2003), President of the Howard Hughes Medical Institute (HHMI), an organization that funds educational reform efforts at many levels.
| A SYSTEMS APPROACH TO TEACHING |
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These two changes, integration of information and utilization of discovery science, are also influencing the way biology is taught. Many departments and curricula are described by old names that have lost much of their meaning: biochemistry, genetics, cell biology. Today, cell biologists use genetics, geneticists use biochemistry, and biochemists use cell biology. Discovery science is fostering a spirit of "discovery education," where students are encouraged to develop insights through interpretation of data (Figure 2). These types of student-based discoveries are at the heart of successful learning promoted by BioQuest and PKAL.
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| TOOLS FOR A SYSTEMS APPROACH TO TEACHING |
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With the rapid pace of science publication, it is difficult for faculty to keep up to date in their chosen fields. PubMed (www.ncbi.nlm.nih.gov/PubMed/) is a productive way to search for key words or authors. A free service called PubCrawler (www.pubcrawler.ie) can automate PubMed searches and deliver periodic search results to your email inbox. Each week I read the titles, linked abstracts, and free PDF files if the paper appeared in one of the many freely available journals (see PubMed Central for a complete listing; www.pubmedcentral.nih.gov). Many campuses have institutional access to major journals such as Science (www.sciencemag.org), Nature (www.nature.com/nature/), and Proceedings of the National Academy of Sciences, USA (www.pnas.org; PNAS). Molecular Biology of the Cell provides free access within 2 months of publication and Genome Biology, PNAS, and Science provide free access within 6 months of publication. When a particularly significant genomics paper is published, Science and Nature often permit immediate free access to the papers, as was the case for the Plasmodium genome sequence (Carlton et al., 2002).
Research papers can be converted easily into case studies for teaching. Online access to papers facilitates the use of real data and figures for reading assignments and classroom lectures. Students benefit when they learn how to interpret real data. Faculty benefit from the dual use of the time spent reading for their research and preparing for class. If we follow the lead of BioQuest, students can be encouraged to ask questions, make discoveries, and discuss their interpretations of current research papers with classmates. Genomics papers that provide public access to the data are ready-made modules for student-based learning and will result in higher levels of thinking (Bloom et al., 1956; Wood, 2002).
Perhaps the greatest benefit of genomics has been the increased number of interdepartmental collaborations. The National Research Council's Bio2010 report (2003) calls for changes in the biology curriculum, but current faculty may find it impossible to teach radically different courses without collaborating. Biologists, especially those trained in cell and molecular biology, will benefit from collaborations with math and computer science colleagues. My own math skills were about as rusty as my German vocabulary, and I wanted to learn more. Fortunately, my institution hired Laurie Heyer, an applied mathematician with training in bioinformatics. Heyer developed a Computational Biology course that was offered in the spring semester (http://www.bio.davidson.edu/courses/compbio/webpage/home.htm) after my first offering of genomics. Half of my genomics students enrolled in her course, where they learned perl programming and applied mathematics to solve biological problems (Figure 4). These seven genomics students were paired with an equal number of math majors who learned some biology and how to apply their knowledge to real-world problems. The course was very popular with the students, and for the first time on my campus, a course was cross-listed in biology and math. Heyer and I collaborate in our research interests as well as our teaching, and we hold joint lab meetings. We were able to model collaboration and demonstrate the value of interdisciplinary training to our students, and we each benefited from each other's insights.
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| GRADING IN A GENOMICS COURSE |
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Web Page Assignments
Popular Press vs. Scientific Press. For their Web page
assignments, students were asked to perform tasks that required evaluation,
application, and synthesis
(www.bio.davidson.edu/courses/genomics/GPBwebstandards.html;
Allen and Tanner, 2002). The
first assignment asked students to compare popular press and scientific
publications about a human gene of their choosing. They were required to
choose a gene that had been called the "smart gene,""fat
gene,""language gene," "gay gene," and so forth.
In addition to initiating the students into the complexity of genomics
compared to genetics, this first assignment ensured that every student knew
how to create Web pages
(www.bio.davidson.edu/Courses/genomics/2002/Henry/popularpress.html).
To assist them, I created a series of Web pages on producing Web pages
(www.bio.davidson.edu/courses/genomics/GPBwebstandards.html#webtools)
and evaluating Internet sources
(www.bio.davidson.edu/courses/genomics/webauthor/evaluate.html).
Describe Two Linked Yeast Genes. The remaining three Web assignments required students to analyze one annotated and one nonannotated gene from the yeast genome (euphemistically termed your favorite yeast genes; YFYG). For the first YFYG assignment, they could select any annotated gene and were encouraged to choose a gene/protein they had studied in another course. However, the nonannotated gene had to be located near their annotated gene (Figure 5). Students learned what they could about their two genes from online DNA resources. The final task was to propose a role for their nonannotated gene based on what they had learned (www.bio.davidson.edu/Courses/genomics/2002/Pierce/yeastgene.htm).
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Describe the Proteins Encoded by YFYG. The final Web assignment focused on the proteomics of their two genes/proteins. Students utilized proteinprotein interaction databases DIP, PathCalling, and Osprey, as well as Gene Ontology, MIPS, SwissProt, Function Junction, etc. (Table 1). On occasion, a student would find meaningful data and formulate plausible hypotheses about his or her nonannotated gene (www.bio.davidson.edu/Courses/genomics/2002/Toran/YOL085Cprotein.html). It was important for students to indicate which databases they used because sometimes they chose genes with little information available and they needed to document this lack of information. Their last task for this assignment was to propose experiments to test their final hypotheses for their unknown genes. They chose genomic or proteomic approaches, as well as more traditional cell and molecular experimental methods. For the most part, these experiments were well designed to test the hypotheses they formulated through their discovery science.
Tests
Genomics does not lend itself to cognitive skills such as memorization (of
genes and sequences) both because high-throughput data are searchable in
databases and because the data could never be memorized. My genomics course
had a prerequisite of genetics so there was no need for me to test students on
basic genetics terminology. As with any scientific field, genomics uses many
specialized terms that students must learn, but I chose to test more than just
vocabulary, though good answers demonstrated a robust vocabulary. In
particular, tests contained questions of comprehension, application, analysis,
synthesis, and evaluation (Allen and
Tanner, 2002; Sundberg,
2002). In my Molecular Biology course I frequently copy and paste
figures from scientific publications for use; however, this approach was not
completely satisfactory. In 2002, I gave students entire papers from
Science or Nature and asked a series of questions about the
paper. As noted above, the best papers for testing purposes included
databases. All exams were open-book, take-home exams that required students to
use the internet extensively. Due to the length of the exams (students
reported taking from 8 to 24 h of dedicated effort to complete the exams),
students were given several days to complete the exams.
I also improved assessment by requiring students to print hard copies of data from Web sites they used to answer questions. Because many of the exam questions had more than one correct answer and/or more than one way to arrive at a correct answer, it was important that I knew what information each student accessed. In addition, students captured screen shots of images to paste into the word processing files to support their answers. Screen shots were particularly useful for answers that utilized color images or protein structures.
I was very pleased with the outcomes of these tests because I felt that I understood how students were thinking. When evaluating their answers, I could see the data they used to formulate their answers. I could determine if they misunderstood the data or if they simply made a bad choice due to ambiguous options from a BLAST search. Here is the test question:
Tell me as much as you can about this sequence [see Figure 7A]. Use as many on-line sites as you want to fill me in on all the scoop. However, to receive maximum points, be sure and tell me every web site/database you visit and what you found there, even if you found nothing. Sometimes that is important information too.
View larger version (120K):
[in this window]
[in a new window]
Figure 7. Example of how student printouts of intermediate steps allow me to recognize an ambiguity in the database search (BLAST; see Appendix A for more information). (A) Sequence students used to determine from which gene the sequence was extracted. (B) Screen shot of BLAST results showing two very similar hits (red lines). (C) E-value calculated for three best hits. (D) Chromosomal map showing the close proximity of the ORF used to extract the sequence (YLR343W) and the upstream gene that also came up as a hit (FSK1).
I encourage you to take screen shots of any graphics you find helpful. Copy and paste these into your Word file.Do not report any information about DNA microarrays for this gene. That will be on the next test.
I had chosen an uncharacterized open reading frame (ORF) from the yeast genome (Figure 7A). Because I knew where I had found the ORF, I did not perform the BLAST search. Surprisingly, when students submitted the sequence, two hits were returned with equal E-values (Figure 7, B and C). One hit was the ORF I had chosen (YLR343W), but the second hit sent students to the gene immediately upstream of the ORF I had chosen (PBR1/FKS1; Figure 7D). Because I had their printed data, I could see how they reached a different answer than the one I "knew" to be right (Appendix A). The first student was initially confused by two gene names for the same gene. Using PubMed and a free online article from the Journal of Bacteriology, however, the student realized that this particular gene had two names. Further student data mining uncovered no orthologs that were consistent with a role in fungal cell wall synthesis. The second example in Appendix A illustrates a different, but also correct answer. This student also used PubMed but was unlucky in choosing which paper to examine. The student dramatically altered her thinking after consulting SGD (Saccharomyces Genome Database; Table 1) and discovering the sequence originated from an unknown ORF and not the better-characterized gene. Using the graphic display at SGD, the student documented that the gene and the ORF were adjacent (Figure 7D and Appendix A). These two students' answers are both correct even though they arrived at different conclusions.
| ASSESSMENT OF STUDENT OUTCOMES |
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Learning Gains
One of the course goals was to introduce students to terms, concepts, and
methods. The average score on the entrance exam (Appendix B) showed how little
students understood at the start of the course, while the average score on the
exit exam showed substantial improvement
(Figure 8). When students began
the class, they were unable to answer basic questions based on genome sequence
variations, DNA microarrays, and proteomics (average score, 0.77 ± 0.1
of 4 possible points), in part because they did not understand the basic
vocabulary. I wrote simple questions for the entrance exam to highlight the
students' lack of prior knowledge in these areas. When the same exam was
administered at the end of the semester, only one student scored 3.5, while
all others scored 4 of 4 possible points (average score, 3.95 ±
0.03).
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Attitude and Self-Perception
At the beginning of the semester, I asked students to email me their
expectations for the course and to describe how they saw themselves within the
field of biology (Appendix C). At the end of the semester, I sent them their
original responses and asked them the same questions again. By not prompting
them on particular topics, I hoped to learn what topics and ideas the students
felt were worth mentioning. Ten of eleven students responded and their
comments were very informative. Below are some of the responses, which have
been clustered under headings for clarity.
Excitement in Learning
I came into the class with little to no understanding of what genomics entailed. ... Now I find myself fascinated by the subject. My friends and family get annoyed with me trying to explain it to them, but I feel like the things I've learned are so revolutionary, I want to share my new found knowledge.
A second student said,
I've never been as interested in the reading and as motivated to continue learning as I have been this semester in Genomics. ... I came in thinking it would be a lot of work that would be difficult to get myself to do; I will leave thinking that it was a lot of work that was enthralling and that I did as willingly as is possible.
Altered Perception of Biology
I never imagined that I would view biology (and science in general) in such a larger context. Before taking this class, I would have to admit that I was prone to looking at areas of biology, like genetics for example, from the "one gene causes one disease" aspect. At times I found myself questioning this approach, but never to the extent to which I do now. I feel as if I've put on a new pair of glasses and can see things more clearly.
Another student supported some of the Bio2010 findings:
It's almost overwhelming to think of the number of different experiments or hypotheses one can synthesize to explain biological phenomena. It's almost more befitting to entitle the course Systems Biology because the course looks at the intimate relationship and, yet, stochastic and independent behavior of the proteome and genome. I wish I could live to be 200 years old and study biology with degrees in physics, chemistry, biology, computer science and mathematics.
Increased Abilities and Confidence
I feel the class has offered me so many opportunities to thrive in the field of biology. Genomics and proteomics are just so relevant to everything that is going on. I feel much more prepared to get a job and apply to grad school than my fellow bio majors at other schools without this background. It is not even so much the material but the willingness to think and learn and question new things.I feel like I have a new range of possibilities for where I go and what I do. I am positive that I want to continue with the field of genomics and proteomics. It is so interesting and malleable to new and innovative ideas. As to my wanting to become more vocal [in class], I feel slight success. What I realized I wanted more was [to] have a better vocabulary to state my ideas. I feel as if I have built a stronger vocabulary in which to communicate intelligently in biological terms.
After taking the exit exam, another student wrote,
This time, not only was I familiar with everything, but I found myself thinking in a different way about the questions. This class has really helped me to think more scientifically. In the past, I had trouble grasping certain facts, especially in genetics, because I knew the material presented (as though it were fully understood and nothing else needed to be considered) had to be more complex. Other times, I couldn't get around the fact that the teacher and the textbook author knew the situation was more complex, yet they chose to simplify it. The awareness of that [unspoken complexity] in my mind resulted in mental roadblocks. ... It is very different in genomics because it seems like we consider everything, and although Occam's razor is often applied, we are always looking for the best explanation, even if it is indeed more complicated than the model.At the beginning of the course, I said I essentially wanted to know more about genomics. I have reached that goal without a doubt, but more and more I have found that this field, including bioinformatics and proteomics, is something that I want to spend a lot more time working on. Its the first time I've really felt confident about my ability to be scientific, but I have a lot more I need to learn. ... So I have new confidence, because I have seen myself improve at biology over 4 years, but I have also found a class that I feel passionate about. I have never immersed myself in a class like I have this one.
Alumni Outcomes
Another way to measure the impact of a course is to follow students after
completing the course. Several graduating students from fall 2001 have taken
jobs in genomics labs due to their increased interest in the field. Some are
in the process of applying for graduate school and one has already been
accepted to an M.D./Ph.D. program, in large part because of her training in
genomics and math. Another student from 2001 was in Bolivia shadowing
physicians on clinical rounds as a part of a postgraduate fellowship. When the
attending physician asked the Bolivian medical students various questions
about cancer biology, my former student was the only one who knew the answers.
She continued by offering a genomics perspective on cancer that we had
discussed in class. As a result, the attending physician asked my former
student to give a guest lecture on the genomics of cancer (in Spanish) to all
medical students the following week. Interest in research is yet another
measure of a course's impact. Six of the 25 students from both years have
conducted genomics research in my lab, while another 3 had to be turned away
due to limited time and resources.
| AREAS FOR IMPROVEMENT |
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One researcher I talked to was ready to offer me a job for the summer the first time he met me if I could do the mathematics and informatics necessary to analyze and interpret the data from his arrays (since his mathematician was leaving for a higher paying job and he had no one else to do it). But I had to be honest and tell him that I could not do the math he wanted me to do. He then went on to tell me that anyone who can do math for these arrays has a job wherever the work is being done. ... So tell your genomics student to start taking math if they want job security!!
| CONCLUSIONS |
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Over the next few years, many institutions will teach genomics. Departments will have to decide whether to blend genomics into existing courses (the way many have done with genetics and molecular biology) or to create new courses. This choice raises an interesting question: Is a genetics course still genetics if it also covers molecular biology, genomics, proteomics, and bioinformatics? At some level, the question of course title is semantics, but for an individual department, the question may require creative solutions when the number of course offerings is limited. Should a separate course in genomics be offered? Based on my experience, student learning outcomes, student self-evaluations, and postgraduate career choices, genomics merits the resources needed to offer independent courses. Perhaps a student response provides the best rationale for creating new genomics courses:
My outlook on biology and even in the way that I think about everyday life is much different. I am constantly finding myself asking questions like'What is the entire effect?' and'How are these things connected and why does that make sense?' My decision to stick with this [genomics] class and put in the hours of time and effort is probably one of the best decisions that I've made in my life.
| APPENDIX A |
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First Example, Where Student Chose One Path with Good Data to Support the Conclusion I first performed a BLASTn with the above sequence. There was 100% identity to part of the S. cerevisiae chromosome XII cosmid 8300. There was 99% identity to the PBR1 gene of S. cerevisiae. There was one gap with this sequence. The S. cerevisiae PBR1 gene for sensitivity to papulacandin B is 5631 bp long, so again, this 660 bp fragment was only a small portion of the gene. Base pairs 1398 of the query also corresponded with a 100% identity to the Saccharomyces cerevisiae 1,3-beta-D-glucan synthase subunit (FKS1) gene, which is the same length as the PBR1 gene. These appear to be the same gene. In fact, when I performed a BLAST2 search with the two sequences, there was a 99% identity. Please see printout.
Before I realized that both genes were the same length, I had thought that perhaps there was some alternative splicing going on with the sequence, but when I inserted the query sequence into ORFfinder, there was only one significant ORF. Which of course now I know corresponds to BOTH genes because they are the same thing.
When I performed a PubMed search of PBR1, I found four hits, but one in particular caught my interest: "Papulacandin B resistance in budding and fission yeasts: isolation and characterization of a gene involved in (1,3)beta-D-glucan synthesis in Saccharomyces cerevisiae" by Castro C, Ribas JC, Valdivieso MH, Varona R, del Rey F, Duran A. A free copy of this paper was located at the Journal of Bacteriology online. In the paper, the investigators characterized the PBR1 gene in S. cerevisiae. According to the paper, PBR1 is identical to the FKS1 gene, which is part of the 1,3-beta-D-glucan synthase complex. (This complex is responsible for the biosynthesis of a major structural component of the yeast cell wall).
It is also interesting to note that in the BLAST results, some human BACs appeared (very small pieces of BACs) and a few other small pieces of other orthologs. However, with these sequences, the E-values are larger, making them not as biologically relevant. It could be just a coincidence that these sequences showed up at all.
Thus, this particular sequence does not appear that this sequence has any major orthologs. The sequence is part of a larger sequence that produces a particular protein that may or may not be in other organisms. It does have a conserved domain (as evidenced when I inserted the amino acid sequence of the PBR1 gene into the conserved domain database). The conserved domain occurs between amino acids 807 and 1632 and corresponds to glucan synthase. According to the conserved domain site, a glucan synthase catalyzes the formation of beta-1,3-glucan polymer, which again is a major component of the fungal cell wall. (Note that the conserved domain is not part of the query sequence; it is merely part of the protein sequence that the query sequence leads to).
Second Example, Where Student Chose a Different Path with Good Data to Support the Conclusion
I began by taking this unknown sequence to the Blastn database. This search
led to a number of hits. Three of these hits appeared to me to be realistic
hits because their E-values were 0 while all other hits had E-values of 0.89
or greater. These three hits were all for yeast. The three red bars were the
yeast hits.
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One hit was for a segment of chromosome 12, the next was for the yeast PBR1
gene on chromosome 12, and the last one was for FKS1 on chromosome 12. This
information I received by clicking on the NCBI links from the BLASTn results
page. In order to determine why these three hits were slightly different I
searched PubMed for PBR1. This gave me one paper about the anti-anti-fungal
properties of PBR1, but no sequence data. I then checked to see if PBR1 is
conserved in humans at GeneCards and the Human Genome Browser and received no
hits for this gene. I figured the next best place to go to learn about yeast
genomics would be SGD. At SGD I performed another BLASTn, this time only of
the yeast genome. This blast found a 100% match on chromosome 12 in the ORF
YLR343W. I next did a FASTA search at SGD and once again found a 100% match to
ORF YLFR343W. I looked at the ORF map of this region of chromosome 12 and was
surprised by what I saw.
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This map shows that our mystery sequence is in ORF YLR343W, the adjacent
ORF to FKS1. Since the original BLASTn data led me to believe that the
sequence was from FKS1 (aka PBR1) I retrieved the full sequence for FKS1 and
YLR343W. It is in fact the case that our sequence is from YLR343W and not from
FKS1. Unfortunatly there is little to nothing known about this ORF. I decided
to take the amino acid sequence provided by SGD for our nucleotide sequence
and perform a BLASTp search. This proved to be circular as the main protein I
found was a hypothetical one based on ORF YLR343W. I next did a Conserved
Domain BLAST with the protein and found that it most closely matched a GAS1
(glycolipid anchored surface protein)
domain.
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I searched NCBI-protein for YLR343W and found a reference to a probably transmembrane protein of the GAS1 family, thus confirming the above diagram's assumption. There is also a reference to it being a probable glycoprotein involved in signaling.
| APPENDIX B |
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Bio111 at Davidson? __________ Genetics? __________ Molecular Biology? __________
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| APPENDIX C |
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I would like you to send me an email by Wednesday with your thoughts. I will keep these emails and then show them to you again at the end of the semester, when I will ask you to summarize your thoughts at that time. I will not grade these, nor use them in any way to evaluate you.
The purpose of this type of evaluation is two fold. First, I am trying to evaluate the effectiveness of certain aspects of my teaching. Second, I hope this self-reflection will enable you to appreciate what you have learned, how you have grown, and what you might do after college.
Finally, I would like your permission to use your comments should I ever publish an article about teaching a genomics course. In your email, please indicate if you grant me permission to quote your responses anonymously.
Last Week of Semester As you end this semester, reflect upon your knowledge in the areas of genomics, proteomics, and bioinformatics. How do you view yourself within the larger context of biology? Did this course meet your expectations?
I would like you to send me an email by Wednesday with your thoughts. I am sending back to you your first response to this request which you submitted back in August. This will serve as a reminder of what you said before class started. I will not grade these, nor use them in any way to evaluate you.
The purpose of this type of evaluation is two fold. First, I am trying to evaluate the effectiveness of certain aspects of my teaching. Second, I hope this self-reflection will enable you to appreciate what you have learned, how you have grown, and what you might do after college.
Finally, I would like your permission to use your comments should I ever publish an article about teaching a genomics course. In your email, please indicate if you grant me permission to quote your responses anonymously.
| ACKNOWLEDGMENTS |
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| FOOTNOTES |
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Corresponding author. E-mail address: macampbell{at}davidson.edu.
| REFERENCES |
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|
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Arbeitman, M.N., Furlong, E.E.M., Imam, F., Johnson, E., Null,
B.H., Baker, B.S., Krasnow, M.A., Scott, M.P., Davis, R.W., and White, K.P.
(2002). Gene expression during the life cycle of Drosophila
melanogaster. Science 297,2270
2275.
Bloom, B.S., Englehart, M.D., Furst, E.J., Hill, W.H., and Krathwohl, D.R. (1956). A Taxonomy of Educational Objectives: Handbook 1: Cognitive Domain. New York: McKay.
Boutanaev, A.M., Kalmykova, A.I., Shevelyov, Y.Y., and Nurminsky, D.I. (2002). Large clusters of co-expressed genes in the Drosophila genome. Nature420,666 669.[CrossRef][Medline]
Campbell, A.M., and Heyer, L.J. (2003). Discovering Genomics, Proteomics and Bioinformatics. Cold Spring Harbor, NY, and San Francisco: Cold Spring Harbor Laboratory Press and Benjamin Cummings.
Carlton, J.M., Angiuoli, S.V., Suh, B.B., et al. (2002). Genome sequence and comparative analysis of the model rodent malaria parasite Plasmodium yoelii yoelii. Nature419,512 519.[CrossRef][Medline]
Cech, T. (2003). Rebalancing teaching and research.
Science 299,165
.
Drosophila Developmental Gene Expression Timecourse (2003). http://genome.med.yale.edu/Lifecycle/. Accessed 23 February 2003.
Dyer, B., and LeBlanc, M. (2002). Meeting Report:
Incorporating genomics research into undergraduate curricula. Cell
Biol. Educ. 1(4),101
104.
LeBlanc, M., and Dyer, B. (2003). Teaching together: A three-year case study in genomics. J. Comput. Small Colleges (in press).
LeBlanc, M., Aspeslagh, G., Buggia, N., and Dyer, B.
(2000). An annotated catalogue of inverted repeats of
Caenorhabditis elegans chromosome III and X with observations
concerning odd/even biases and conserved motifs. Genome
Res. 10(9),1381
1392.
National Research Council, Committee on Undergraduate Biology Education to Prepare Research Scientists for the 21st Century. (2003). BIO2010: Transforming Undergraduate Education for Future Research Biologists. Washington, DC: National Academies Press.
PKAL. (2003a). What works statements. http://www.pkal.org/template1.cfm?c_id=253. Accessed 2 February 2003.
PKAL. (2003b). Characteristics of a good network from the PKAL experience. http://www.pkal.org/template2.cfm?c_id=100. Accessed 2 February 2003.
Shiflet, A.B. (2003). Computational science. http://www.woffordcollege.org/ecs/. Accessed 2 February 2003.
Shiflet, A.B., and Shiflet, G.W. (2002). Computational science in a liberal arts college. J. Comput. Sci. Colleges 18,157 168.
Sundberg, M.D. (2002). Assessing student learning.
Cell Biol. Educ. 1,11
15.
Uno, G.E. (1998). Handbook on teaching undergraduate science courses. Brooks/Cole.
Wood, W.B. (2002). Genesis of biochemistry: A problems
approach. Cell Biol. Educ. 1,16
17.
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S. K. Flowers, C. Easter, A. Holmes, B. Cohen, A. E. Bednarski, E. R. Mardis, R. K. Wilson, and S. C.R. Elgin Genome Science: A Video Tour of the Washington University Genome Sequencing Center for High School and Undergraduate Students CBE Life Sci Educ, December 1, 2005; 4(4): 291 - 297. [Abstract] [Full Text] [PDF] |
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A. Kumar Teaching Systems Biology: An Active-learning Approach CBE Life Sci Educ, December 1, 2005; 4(4): 323 - 329. [Abstract] [Full Text] [PDF] |
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A. E. Bednarski, S. C.R. Elgin, and H. B. Pakrasi An Inquiry into Protein Structure and Genetic Disease: Introducing Undergraduates to Bioinformatics in a Large Introductory Course CBE Life Sci Educ, September 1, 2005; 4(3): 207 - 220. [Abstract] [Full Text] [PDF] |
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