4.6—Plant biology is better understood than Smith seems to think it is

Successful plant breeding relies on thorough understanding of the whole organism’s response to genetic modification.

See Genetic Roulette’s False Claims at Bottom of Page

Analysis of Peer-Reviewed Research:

Plants are shaped by evolution to generally tolerate considerable disruption of chromosomal structure, but in reading this section of Smith’s book we would never know that. What’s more, he incorrectly links the way genes are organised on a plant chromosome with the way they participate in plant regulatory circuits, which means his risk assessment is quite unrealistic.

To understand how unrealistic his risk assessment unit is one needs to realise that for participation in a regulatory network genes do not have to be located on the chromosome in a pattern that maps the organisation of the network. Because genes and plant regulatory networks are distinct from one another, closely coordinated genes can be widely separated from one another on chromosomes and still work together effectively and in many crop plants (maize for instance) much of the DNA does not contain genes. Insertion of a new DNA into a chromosome will not unavoidably disrupt a plant regulatory network. This section of Genetic Roulette also fails to mention current agricultural biotechnology research focused on identifying and exploiting complicated biological regulatory networks to breed better crops such as drought tolerant corn. This sits rather oddly with Smith’s portrayal of plant biotechnologists as being ignorant of new concepts about how complex regulatory circuits operate in plants.

1. Improvement of performance of agricultural crops demands a thorough understanding of how plants behave in cropping systems. The standard training of biologists who undertake research and development of agricultural crops involves comprehensive grounding on how plants work in both greenhouse and field situations. Current research on improvement of crops involves dissection of plant responses to various stress caused by a lack of water, restricted nitrogen availability, or high temperature. Gene chips, for instance, are being used to follow the responses of whole sets of genes inside the plant to disruptive environmental changes, and to reveal the full range of changes going on inside the plant that form part of the full biological response to stress.  Not only are modern plant biotechnologists aware of the complicated interactions between genes and cell regulatory circuits, they are actively dissecting them and using them to develop more water efficient crops (Mentzen and Wurtele 2008, Oh and others (2005).   Pellegrineschi  and others (2004),  Umezawa T and others (2006), Yamaguchi-Shinozaki K and Shinozaki 2006).  Perturbations to plant behavior by transgene insertions are unlikely to be ignored by agricultural biotechnologists because appropriate recognition of them determines the success or failure of new varieties of crops in the field. Genetic Roulette provides very little of this background.

2. Plants have resilient genomes that have survived from millions of years while constantly being bombarded with random disruptions. Jeffrey Smith claims that “a random insertion with its associated mutations and deletions might wreak havoc throughout a network of finely tuned and coordinated genes”. Smith doesn’t mention that the distinctive characteristic of flowering plants is the way they can tolerate radical and extensive changes to their chromosomes (Dooner and Weil 2007, Kidwell and Lisch 2002, Leitch and Leitch 2008, Rutgers University Press Release 4th Oct 2006). Unlike animals, in plants the addition of two complete sets of chromosomes from different species often leads to the creation of a new species — for example cereal wheat– that is a fertile and successful hybrid organism despite the radical genetic stress that this generates (Kashkush and others 2002,  Kashkush and others 2003). During such hybridisation events, and after other genetic disruptions suffered by plants, such as damage to chromosomes by radiation, there are extensive rearrangements of plant DNA (Gorbunova and Levy 1999, Shirley and others 1992). As far plants are concerned, it seems such radical genetic changes are just another day at the office.

3. Many genetic changes have no effect on the way a plant behaves. Practical experience of plant geneticists reveals that most insertions of new DNA in plant chromosome have little effect on other genes (Bouché  and Bouchez  2001). After acknowledging that there can be complicated interactions between genes, and that DNA insertion might influence regulatory networks involved in many genes, it also should be remembered that the original discovery of genes was only possible because disruption of a gene causes a limited set of changes to the organism, such as a change in eye colour. Also many parts of the plant genome do not appear to contain genes. In maize for example, genes take up only some 20% of the total genomic DNA (San Miguel and others 1996). Plant scientists do not make an assumption that genes are isolated units that do not interact with other genes (as wrongly implied by Smith), but they do know from practical experience that many genetic changes to chromosomes influence only one particular trait, and do not necessarily have broad influence on the plant.

4. The arrangement of genes on the chromosome is not a map of the plant’s regulatory circuits. Jeffrey Smith argues that the disruption of gene arrangements that occurs when a transgene is inserted will necessarily disturb regulatory networks that govern the way plants survive. But genes are not simply a picture of how the cell and organism works. They are more like pages in a recipe book rather than final cake. Just like you can still cook brilliantly successful meals using a recipe book with notes stuck on the pages, so it is that by changing gene arrangements you don’t necessarily change the regulatory networks of the plant.

5. Plant biologists have long known that clusters of genes can do related tasks. Smith quotes an article by Lawrence Hurst (Hurst and others 2004) to argue that only recently has the clustering of genes with related functions in chromosomes being recognised, and that biotechnologists ignore this concept. Smith takes this quote out of context with a representation of scientific opinion that is simplistic and distorted. Hurst’s article makes it clear that the idea that biologists assume that genes are always randomly organised in chromosomes is his own deliberate rhetorical exaggeration (he uses the term “strawman”). Realistically, biologists do not have the simplistic opinion that they are portrayed as having by Smith.

References

Bouché N and Bouchez D (2001) Arabidopsis gene knockout: phenotypes wanted. Curr Opin Plant Biol. 2001 Apr;4(2):111-117 A survey of many insertions shows most DNA insertions do not change the plant phenotype.

Dooner HK and Weil CF (2007). Give-and-take: interactions between DNA transposons and their host plant genomes. Current Opinion in Genetics & Development 2007, 17:486–492. The interaction of chromosomes and mobile DNA elements (transposons) has rearranged genes, shuffled regulatory sequences, mobilise genes to new locations and added new genes to plants.

Gorbunova V and Levy AA (1999). How plants make ends meet: DNA double-strand break repair. Trends in Plant Science 4(7):263-269. Plants have particularly error-prone mechanisms that join together bits of broken chromosomes. These repair mechanisms scramble the DNA at the site at which the chromosomes are joined together during their repair. Radiation is a common cause of broken chromosomes and triggers these processes which scramble plant DNA and cause mutations.

Hurst LD, Pál C and Lercher MJ (2004). The evolutionary dynamics of eukaryotic gene order. Nature Reviews Genetics 5:299-310. Often neighbouring genes to similar things.

Jiang N, Bao Z, Zhang X, Eddy SR and Wessler SR (2004) Pack-MULE transposable elements mediate gene evolution in plants. Nature 431, 569-573. Mobile DNAs in rice carry fragments of more than 1000 cellular genes.

Kashkush K, Feldman M, and Levy AA (2002). Gene loss, silencing and activation in a newly synthesised a wheat allotetraploid. Genetics 160:1651-1659. The history of safe use of genetics, with more information on the unexpected genetic changes that occurred during crop evolution. The re-enactment of the evolution of wheat to shows that when the two component grasses cross hybridised, many genes were silenced, activated, and some were lost.

Kashkush K and Feldman M, and Levy AA (2003).Transcriptional activation of retrotransposons alters the expression of adjacent genes in the wheat. Nature Genetics 33:102-106. Documentation of unexpected genetic changes that occur with conventional plant breeding. Following cross hybridisation between different grasses, both activation and silencing of genes takes place.

Kidwell MG and Lisch DR (2002). Transposable elements as sources of genomic variation. Chapter 5 in NL Craig and others. Mobile DNA II. ASM Press.

Lai J Li Y and Messing J, Dooner HK. (2005) Gene movement by Helitron transposons contributes to the haplotype variability of maize. Proceedings of the National Academy of Sciences of the USA 102(25):9068-73. Active shuffling of DNA in corn is catalysed by numerous parasitic DNAs.

Lisch D (2005). Pack-MULEs: theft on a massive scale. Bioessays 27:353-355. In rice thousands of genes in portions of genes have been duplicated, transposed and rearranged by the activities of a family of mobile DNA that is called MULE.

Leitch AR and Leitch IJ (2008). Genome plasticity and the diversity of polyploid plants.Science 320:481-483 The success of flowering plant is partly attributable to their highly plastic genomes which can withstand large scale changes in structure over just a few generations.

Mentzen WI and Wurtele ES (2008). Regulon organization of Arabidopsis. BMC Plant Biol. 30;8:99. Gene chips are used to find the regulatory groupings in the mustard cress plant. www.biomedcentral.com/content/pdf/1471-2229-8-99.pdf accessed Dec 26 2008. Gene chips used to follow grouping of genes that are active together. Often neighbouring genes  turn on together.

Oh SJ, Song SI, Kim YS, Jang HJ, Kim SY, Kim M, Kim YK, Nahm BH and Kim JK  (2005). Arabidopsis CBF3/DREB1A and ABF3 in transgenic rice increased tolerance to abiotic stress without stunting growth. Plant Physiol 138:341-351

Pellegrineschi A, Reynolds M, Pacheco M, Brito RM, Almeraya R, Yamaguchi-Shinozaki K and Hoisington D (2004). Stress-induced expression in wheat of the Arabidopsis thaliana DREB1A gene delays water stress symptoms under greenhouse conditions. Genome 47:493-500.

Rutgers University Press Release (4th Oct 2006). Genome archaeology illuminates the genetic engineering debate. www.eurekalert.org/pub_releases/2006-10/rtsu-gai100306.php%20accessed%20Dec%2011%202008. Summarising Bruggmann and others Genome Research 16:1241-1251. The maize genome is “replete with reconfiguration and reshuffling, reminiscent of working with Lego blocks”.

SanMiguel P, Tikhonov A, Jin YK, Motchoulskaia N, Zakharov D, Melake-Berhan A, Springer PS, Edwards KJ, Lee M, Avramova Z and Bennetzen JL (1996). Nested retrotransposons in the intergenic regions of the maize genome  Science 274(5288):765 – 768

Shirley BW, Hanley S and Goodman HM (1992). Effects of ionizing radiation on a plant genome: analysis of two Arabidopsis transparent testa mutations. The Plant Cell 4, 333-347. Demonstration that mutations induced by radiation contain radically scrambled DNA.

Umezawa T, Fujita M, Fujita Y, Yamaguchi-Shinozaki K and Shinozaki K (2006). Engineering drought tolerance in plants: discovering and tailoring genes to unlock the future. Curr Opin Biotechnol. 17(2):113-22. Recent studies have increased our understanding of the regulatory networks controlling the drought stress response and have led to practical approaches for engineering drought tolerance in plants.

Yamaguchi-Shinozaki K, Shinozaki K (2006). Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol. 57:781-803. “Recent progress has been made in analyzing the complex cascades of gene expression in drought and cold stress responses, especially in identifying specificity and cross talk in stress signaling. In this review article, we highlight transcriptional regulation of gene expression in response to drought.”