Freeling, Michael

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CREA Journals (Consiglio per la ricerca in agricoltura e l’analisi dell’economia agraria)

Open AccessMaydica 57-2012Commentaryreceived 09/19/2012Response to Birchler: Heterosis is partly a sub-problem of quantitative genetics, but its solution may depend on understanding the mysterious genetics of quantityMichael FreelingDepartment of Plant and Microbial Biology, UC-Berkeley, Berkeley, CA 94720 USAE-mail: freeling@berkeley.eduJim Birchler, in his thoughtful and cautionary commentary on heterosis, de-duces from the literature that we can be reasonably sure that heterosis is a positive quantitative trait, and not the complementation of weakly deleterious alleles. Indeed, the reason this conclusion “might seem to be a small step forward” is not only that it is, but that the term “quantitative genetics” im-plies that heterosis (and it’s opposite phenomenon, inbreeding depression) is an emergent property of many, many genes, genes expected to follow the rules of polygenic inheritance. This implication is not necessarily true because the “genes” might well be rapidly changeable pairs of epialleles, these falling under no known theory. There have been reports that smallRNA levels are not within the range of parental values in wide plant hybrids (Barber et al, 2012; Groszmann et al, 2011; Kenan-Eichler et al, 2011; Shen et al, 2012). Inbreed-ing depression may disappear in RMR1 knockouts along with many 24 nt smRNAs (Hale et al, 2009). On grand average, 24 nt RNAs are often depleted in the hybrid. Small RNAs of this sort are usually associated with directing methylation and generally suppressing expression—totally or partially-- so the soma of the hybrid would be expected, on grand average, to be temporarily over-expressing some transposons and perhaps some genes. A particularly important pair of papers by Hollister and Gaut (Hollister and Gaut, 2009; Hollister et al, 2011)(Brandon Gaut lab) com-pare gene expression between Arabidopsis thaliana and the comparatively transposon-rich Arabidopsis lyrata; they found an association between methyl-ated transposons near genes and down-regulation of those genes, as if there were a whole genome trade-off between transposon silencing and steady state RNA levels. This “trade-off hypothesis” employs small RNAs to initiate and reinforce methylation. Do changes in smRNAs in the somas of wide hybrids really cause a cascade of gene regulation that ends with a one-time-only heterotic growth burst, or are they only associated with diverged parents and their hybrids? Birchler cautions us that confusing correla-tion for cause is not only ignorant and fallacious, but may be disrespectful of the long history of geneticists not solving heterosis. Respect is good, but discover-ing something new is better, and a bit of disrespect might sweeten the quest. Just because an idea has not been proved to explain heterosis does not mean that it is not true. It is or it isn’t. If the new idea or as-sociation helps you imagine, it’s beautiful to you. My beautiful ideas about inbreeding depression and hybrid vigor are those that address heterosis as a transient, emergent property of two genomes si-multaneously come together in the same nucleus by chance, genomes that evolved for some considerable period within their parental genomes, periods with different DNA/DNA-modification birth/death histo-ries. I’m astounded by the diversity among maize in-breds for the quantitative levels of gene expression (in FPKM in normalized RNAseq experiments) acquired by genes after just a few or several thousand genera-tions (Hansey et al, 2012). We don’t know how genes are quantitatively modulated explaining adequately balanced gene expression over the entire transcrip-tome of an organ or organ system, but this diversity must be acquired/lost very quickly, and transposon blooms and position effects are particularly fast. This evolutionary speed aspect is what makes Hollister and Gaut’s trade-off model of transposon silencing versus gene expression particularly useful (beautiful, but not proved). Research on genome dominance, where two parental genomes going into a wide-cross tetraploidy end expressed to different average mRNA levels (Flagel and Wendel, 2010; Schnable et al, 2011), also implicates fast whole-genome gene expression modulation. The clue: whole genomes can quickly al-ter overall levels of many individual gene expressions. My lab’s conceptual solution to the heterosis prob-lem (extrapolated from Hollister and Gaut’s trade-off model to explain our own data) involves the genetics of mRNA quantity, is testable, and is presented as a cartoon to amuse our critics (Freeling et al, 2012). Our model hypothesizes that inbreeding expression = genome dominance. It is always the time for academic rigor. But, now is the time to put the old ideas of quantitative inheri-Maydica 57 ~ 96-97Michael Freeling 97Maydica electronic publication - 2012tance out of the way, try to do something about our ignorance of the genetics of mRNA quantity and fol-low the other enigmatic but beautiful new clues to-ward solving the heterosis / inbreeding depression problem.AcknowledgementsFunded by NSF Plant Genome Research ProgramProfessor of GeneticsReferencesBarber WT, Zhang W, Win H, Varala KK, Dorweiler JE et al, 2012. Repeat associated small RNAs vary among parents and following hybridization in maize. Proc Natl Acad Sci USA 109: 10444-10449Flagel lE, Wendel JF, 2010. Evolutionary rate varia-tion, genomic dominance and duplicate gene expression evolution during allotetraploid cotton speciation. New Phytol 186: 184-193Freeling M, Woodhouse MR, Subramaniam S, Turco G, Lisch D et al, 2012. Fractionation mutagenesis and similar consequences of mechanisms remov-ing dispensable or less-expressed DNA in plants. Curr Opin Plant Biol 15: 131-139Groszmann M, Greaves IK, Albertyn ZL, Scofield GN, Peacock WJ et al, 2011 .changes in 24-nt siRNA-levels in Arabidopsis hybrids suggest an epigen-etic contribution to hybrid vigor. Proc Natl Acad Sci USA 108: 2617-2622Hale CJ, Erhard KF jr, Lisch D, Hollick JB, 2009. Pro-duction and processing of siRNA precursor tran-scripts from the highly repetitive maize genome. Plos Genet 5: e1000598Hansey CN, Vaillancourt B, Sekhon RS, De leon N, Kaeppler SM et al, 2012. Maize (Zea mays L.) Ge-nome diversity as revealed by RNA-sequencing. Plos One 7: e33071Hollister JD, Gaut BS, 2009. Epigenetic silencing of transposable elements: A trade-off between re-duced transposition and deleterious effects on neighboring gene expression. Genome Res 19: 1419-1428Hollister JD, Smith IM, Guo YL, Ott F, Weigel D et al, 2011. Transposable elements and small RNAs contribute to gene expression divergence be-tween Arabidopsis thaliana and Arabidopsis ly-rata. Proc Natl Acad Sci USA 108: 2322-2327Kenan-eichler M, Leshkowitz D, Tal L, Noor E, Melamed-Bessudo C et al, 2011. wheat hybrid-ization and polyploidization results in deregulation of small rnas. Genetics 188: 263-272Schnable JC, Springer NM, Freeling M, 2011. Differ-entiation of the maize subgenomes by genome dominance and both ancient and ongoing gene loss. Proc Natl Acad Sci USA 108: 4069-4074Shen H, He H, Li J, Chen W, Wang X et al, 2012. Ge-nome-wide analysis of DNA methylation and gene expression changes in two Arabidopsis ecotypes and their reciprocal hybrids. Plant Cell 24: 875-892

Response to Birchler: Heterosis is partly a sub-problem of quantitative genetics, but its solution may depend on understanding the mysterious genetics of quantity

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Response to Birchler: Heterosis is partly a sub-problem of quantitative genetics, but its solution may depend on understanding the mysterious genetics of quantity

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