What is the dominant view of junk DNA?

I think that about 90% of our genome is junk and I know lots of other scientists who feel the same way. I'm pretty sure that this view is not shared by the majority of scientists but I don't know whether they are convinced that most of our genome is functional or whether they just think the question is unanswerable at the present time. I suspect that the latter view is more common but I'd like to hear your opinion.

How much of our genome is junk? The three most obvious answers are:

1. Most of our genome is junk
2. Very little of our genome is junk
3. We don't know enough to answer the question

I recently bought the latest edition of Introduction to Genomics by Arthur M. Lesk to see how he treats genome composition. This is the third edition of a book that was first published in 2007 and it's a excellent book for learning about the common techniques in the field of genomics. However, it's not so good when it comes to discussing the big picture, especially with respect to the human genome. There's no discussion about the overall composition of our genome and how much of it is junk and no mention of the evidence supporting junk DNA. Nevertheless, the position of the author seems clear from the following passages. He is a supporter of option #3 and I suspect that's the majority opinion these days.

Approximately 5% of the dog genome constitutes functional elements common to dog, human, and mouse. This is higher than the protein-coding fraction of the human genome. It includes regulatory elements and non-protein-coding RNAs, and further suggests that it is premature to dismiss as 'junk' the regions of the genome to which we cannot yet assign function. (p. 225)

Five Things You Should Know if You Want to Participate in the Junk DNA DebateThe fact that we can assign function to more than protein-coding regions is hardly a new idea so I don't know why he makes such a big deal of this fact. Furthermore, the idea that we dismiss as junk any DNA to which we cannot assign function is a serious misrepresentation of the junk DNA position. I think it reflects a general lack of understanding of the evidence for junk DNA [Required reading for the junk DNA debate].

Regions of the genome without known function are often referred to as 'junk DNA'. Of course, the fact that we may not know the function of much of our genome does not mean that it has none. (Maybe it is junk, but it is certainly not transcriptionally inert. A series of recent discoveries has revealed many new types of RNA molecules, mostly involved in control processes. It would be naïve to doubt that many more types will come to light.) Moreover, the amount of space between genes affects the rate of crossing over and recombination and, thereby, rates of evolution. Indeed, the large amount of repetitive sequence between our genes enhances recombination rates by promoting homologous recombination. Rate of evolutionary change is characteristic of a species that is certainly subject to selective pressure. Features of the genome that affect rate of evolution cannot be dismissed entirely as junk. (p. 239)

I bet Joe Felsenstein will have something to say about selection for high rates of evolution by inserting spacers between genes. He can probably think of one or two faster, more efficient, ways of enhancing recombination if that were necessary to speed up evolution.

Traditionally, DNA outside protein-coding regions was considered 'junk', but for no reason other than ignorance. ... There has been extensive and heated debate over the classification of transcripts as functional without being able to assign specific functions to them. Part of the problem is that many transcripts for which unspecified function was claimed do not show conservation among mammals. This was the basis for many criticisms of the claims of the ENCODE consortium in its early publications. The rule, which certainly applies to proteins, that nature conserves important things but not unimportant things, does not necessarily apply to these transcripts. Sequence-structure-function relationships can be very different for RNAs and for proteins. The argument that transcribed regions are functional—rather than just 'junk RNA'—rests on the observation of differential transcription in cell-specific patterns, and dynamic regulation of transcription during development and tissue differentiation and disease. (p. 359)

As we have discussed many times, the idea that different transcripts are expressed in different cells is perfectly consistent with spurious transcription due to inappropriate binding of tissue-specific transcription factors. It is not evidence of function. Furthermore, lack of conservation is powerful evidence against function and it should not be dismissed lightly.

I think these passages reveal the true fall-back position after the ENCODE fiasco. Scientists like Arthur Lesk are reluctant to adopt the position that most of our genome is functional because of the controversy but they reject the idea that most of our genome is junk because they think it's based on ignorance. They assume an intermediate position where they claim that that we just don't know enough about our genome to decided whether it is full of functional elements or not.¹

I believe that this position will not stand up to close scrutiny but that's not the point. My point is that I think this is the dominant view of junk DNA. What do you think?

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1. I suspect that almost everyone who argues for option #3 is a closet functionalist.