Polyploidy – from evolution to development?

by Rainer Melzer
School of Biology and Environmental Science and Earth Institute, University College Dublin

A large variety of molecular mechanisms regulate developmental processes. Transcription factors entered the stage already decades ago and are still widely considered master regulators of development (Wray et al., 2003). However, in the past years it has been demonstrated that many other biomolecules play pivotal roles in development. This includes histone modifying complexes, small RNAs and long          noncoding RNAs (Holoch and Moazed, 2015, Venkatesh and Workman, 2015). In almost all those cases, the developmental importance of a regulatory mechanism is demonstrated first. This is often then followed by evolutionary considerations and phylogenetic studies. For example, transcription factors now play a central role in evo-devo research, and changes in transcription factor function are proposed to have played important roles in the evolution of plant and animal body plans (Cheatle Jarvela and Hinman, 2015, Rodríguez-Mega et al., 2015). Likewise, microRNAs have been implicated in major evolutionary transitions (Peterson et al., 2009).

In contrast to those regulatory molecules, another mechanism that has far-reaching consequences for cellular processes has mainly been discussed in the ecological and evolutionary arena: polyploidy (Ramsey and Ramsey, 2014). The doubling of the entire genome has long been implicated in the origin of new species or even entire new clades. Polyploidy has recently gained even more attention with the discovery that many plant lineages underwent polyploidization events in the past. Current evidence indicates that polyploidization is associated with an increase in diversification rates and possibly also with the origin of evolutionary novelties (Schranz et al., 2012, Landis et al., 2018).

OrchidFlower Rainer Melzer Compared to the importance of polyploidy in evolutionary research, it has gained relatively little attention in plant developmental biology. This is to some extent surprising, as it is well established that different somatic cells of a plant can differ in their ploidy level (Traas et al., 1998). At the same time, it is also known that there is a direct relationship between e.g. the size of a cell and its ploidy level (Traas et al., 1998). Thus, heterogeneity at the cell level and phenotypic output might be directly linked.               Bateman et al., (2018) explored this link between polyploidy and developmental patterning further by analysing orchid flowers. Orchids are an especially interesting study subject as the floral structure of many orchids is quite elaborate, showing extensive micromorphological diversification. Thus, one question that arises is whether those intricate morphologies are in part brought about by different ploidy levels in different cells.
Bateman and colleagues used microscopy to measure the size of nuclei in different regions of the labellum – a highly specialized petal-like organ of orchids. They complemented those studies with flow cytometry, which provides an independent and more quantitative estimate of nuclear genome sizes in different organs, but lacks the cellular resolution of microscopic measurements (Bateman et al., 2018).

Intriguingly, the authors find significant variations of the ploidy level depending on the labellum region. Polyploidy was especially pronounced in trichomes of the labellum. Those trichomes were also among the largest and most complex cells analysed, confirming that there might be a direct link between cell size and ploidy level. In addition, the flow cytometry data provided some evidence that the ratio between different ploidy levels is tissue- and organ-specific, with leaf material showing a relatively high percentage of diploid and tetraploid nuclei whereas in the labellum diploid nuclei were very rare and higher ploidy levels dominated (Bateman et al., 2018). Also, different labellum regions showed different flow cytometry signatures, indicating that some kind of ‘ploidy code’ might be applicable to distinguish different organs and tissues.

The authors further speculate that the size increase often observed in polypoid cells might, if cells are embedded in a tissue, lead to local distortions that may in turn contribute to the elaborate three-dimensional structure of many orchid labella. Interestingly, data from giant polyploid cells in Arabidopsis sepals support this notion. In this case, the large cells are required for the curvature of the sepals (Roeder et al., 2012).

The study of Bateman et al., (2018) provides an exciting starting point for further research. After polyploidy research has taken evolutionary biology by storm the time seems right to explore its relevance for developmental mechanisms.

References

Bateman RM, Guy JJ, Rudall PJ, Leitch IJ, Pellicer J, Leitch AR. 2018. Evolutionary and functional potential of ploidy increase within individual plants: somatic ploidy mapping of the complex labellum of sexually deceptive bee orchids. Annals of Botany 122: 133-150. doi: 10.1093/aob/mcy048

Cheatle Jarvela AM, Hinman VF. 2015. Evolution of transcription factor function as a mechanism for changing metazoan developmental gene regulatory networks. EvoDevo 6: 3. https://doi.org/10.1186/2041-9139-6-3

Holoch D, Moazed D. 2015. RNA-mediated epigenetic regulation of gene expression. Nature Reviews Genetics 16: 71. doi: 10.1038/nrg3863

Landis JB, Soltis DE, Li Z, Marx HE, Barker MS, Tank DC, Soltis PS. 2018. Impact of whole-genome duplication events on diversification rates in angiosperms. American Journal of Botany 105: 348-363. https://doi.org/10.1002/ajb2.1060

Peterson KJ, Dietrich MR, McPeek MA. 2009. MicroRNAs and metazoan macroevolution: insights into canalization, complexity, and the Cambrian explosion. Bioessays 31: 736-47. https://doi.org/10.1002/bies.200900033

Ramsey J, Ramsey TS. 2014. Ecological studies of polyploidy in the 100 years following its discovery. Philosophical Transactions of the Royal Society B: Biological Sciences 369.

Rodríguez-Mega E, Piñeyro-Nelson A, Gutierrez C, García-Ponce B, Sánchez MDLP, Zluhan-Martínez E, Álvarez-Buylla ER, et al. 2015. Role of transcriptional regulation in the evolution of plant phenotype: A dynamic systems approach. Developmental Dynamics 244: 1074-1095. https://doi.org/10.1002/dvdy.24268

Roeder AHK, Cunha A, Ohno CK, Meyerowitz EM. 2012. Cell cycle regulates cell type in the Arabidopsis sepal. Development 139: 4416-4427.

Schranz EM, Mohammadin S, Edger PP. 2012. Ancient whole genome duplications, novelty and diversification: the WGD Radiation Lag-Time Model. Current Opinion in Plant Biology 15: 147-153. https://doi.org/10.1016/j.pbi.2012.03.011

Traas J, Hülskamp M, Gendreau E, Höfte H. 1998. Endoreduplication and development: rule without dividing? Current Opinion in Plant Biology, 1: 498-503. https://doi.org/10.1016/S1369-5266(98)80042-3

Venkatesh S, Workman JL. 2015. Histone exchange, chromatin structure and the regulation of transcription. Nature Reviews Molecular Cell Biology 16: 178. http://dx.doi.org/10.1038/nrm3941

Wray GA, Hahn MW, Abouheif E, Balhoff JP, Pizer M, Rockman MV, Romano LA. 2003. The evolution of transcriptional regulation in eukaryotes. Molecular Biology and Evolution 20: 1377-1419. https://doi.org/10.1093/molbev/msg140

Advertisements

About Flowering Highlights

Flowering Newsletter published by the Journal of Experimental Botany
This entry was posted in flowering and tagged , , , , . Bookmark the permalink.

Leave a Reply

Fill in your details below or click an icon to log in:

WordPress.com Logo

You are commenting using your WordPress.com account. Log Out /  Change )

Google+ photo

You are commenting using your Google+ account. Log Out /  Change )

Twitter picture

You are commenting using your Twitter account. Log Out /  Change )

Facebook photo

You are commenting using your Facebook account. Log Out /  Change )

Connecting to %s