How much fruit is in a flower?
By Diarmuid Ó Maoiléidigh
Comparing apples and oranges
The variety in the flavor and form of fruits is astounding, although we rarely stop to consider how their form relates to the flower from which they grow. Oranges and peaches (the latter were called Persian apples by the Romans) are summer favorites but an orange contains discreet segments with a seed in most segments while a peach is a single mass of fleshy fruit containing a single seed. The difference between the forms of these fruits can be traced back to the flower.
In flowering plants, the female reproductive structure (the gynoecium) is fertilized by pollen shed from the male reproductive structure (the anther). The gynoecium is made of individual units termed carpels, which contain one or more ovules ready to be fertilized to generate seeds. In oranges, the gynoecium contains ten carpels whereas peaches only bear one carpel per gynoecium. The number of carpels that a flower produces depends on the size of the stem cell population within the flower. Changing the size of this stem cell population is an effective target for breeding and genetic engineering in order to increase fruit size and yields.
New research from Norbert Bollier and colleagues (2017) provides a platform to manipulate tomato fruit size and yield.
Meristems, flowers and fruits
Stem cells have a very special property in that they can change into any cell of the body if they receive the right signals. In plants, these stem cells are contained within regions called meristems. Meristems, and therefore the stem cells within them, can self-renew, which means that plants can continue to grow as long as the stem cell population does not dwindle. Ancient Redwood trees, for example, need to maintain their meristems in order to continue growing. We can consider there to be three major zones containing meristems in the plant: in the root, the shoot, and the flower. Unsurprisingly the root meristem is important to provide cells for root growth, the shoot meristem contributes to all the above ground tissue (leaves, stems etc.) while the flower meristem directly contributes to the formation of most floral organs. Although the root and shoot meristems are able to continue growing under the right conditions, the floral meristem stops growing once the flowers are formed. In fact, the formation of the carpels and the longevity of floral meristem are tightly linked.
How do we turn off the floral meristem?
Plant biologists use several organisms as models to help establish what might be happening in more complex plants that are important for agriculture. The most popular and well-studied model is Arabidopsis thaliana, which is part of the mustard family. A lot of research has been done in Arabidopsis to understand how the size of the floral meristem is controlled. One of the first genes to be cloned in Arabidopsis was AGAMOUS, which controls the formation of stamens and carpels. The floral meristems within plants lacking AGAMOUS activity stay active for much longer (Lenhard et al., 2001). The AGAMOUS gene codes for a transcription factor, a protein that can turn on and off other genes by interacting with them. One of the genes that AGAMOUS switches on is called KNUCKLES and plants lacking KNUCKLES activity also bear floral meristems that remain active for longer than normal (Payne et al., 2004; Sun et al., 2009). The KNUCKLES protein forms a complex with other proteins including the MINI ZINC FINGER 2 protein. MINI ZINC FINGER 2 and KNUCKLES are both transcription factors and they act to turn off the expression of WUSCHEL, whose activity controls the lifespan of the floral meristem.
From basic research to your kitchen table
Bollier et al. show that all the genes mentioned above are present in tomato as well as Arabidopsis, and that they perform the same functions in both species. This was not necessarily expected because the two species are not closely related. This information provides biologists with a clear strategy to improve tomato fruit size and yield: stop WUSCHEL from being switched off too early. We know that this strategy can be effective, because WUSCHEL activity is prolonged in domesticated tomato compared to wild tomato species, and in certain tomato mutants that produce larger fruits (Xu et al., 2015). The work discussed here provides a means of achieving this end that can be targeted in a directed manner in order to improve yields in tomato. One promising approach is to remove the DNA sites in the WUSCHEL gene that KNUCKLES and MINI ZINC FINGER 2 use to inactive it. This strategy is also likely be transferable to some other crop species since a similar mechanism to control floral meristem activity may be evolutionarily conserved.
Diarmuid Ó Maoiléidigh
Department of Developmental Biology
Max Planck Institute for Plant Breeding Research
Cologne, Germany
ORCID: 0000–0002–3043–3750
Email: omaoil@mpipz.mpg.de
Read the research article upon which this story is based:
Bollier N., Sicard A., Leblond J., Latrasse D., Gonzalez N., Gévaudant F., Benhame M., Raynaud C., Lenhard M., Chevalier C., Hernould M., and Delmas F. (2018) AtMIF2 and SlIMA 1 proteins, a Conserved Missing Link in the regulation of Floral Meristem Termination in Arabidopsis and Tomato. The Plant Cell, published January 2018 https://doi.org/10.1105/tpc.17.00653
Other cited references:
Lenhard M., Bohnert A., Jürgens, G. and Laux T. (2001) Termination of Stem Cell Maintenance in Arabidopsis Floral Meristems by Interactions between WUSCHEL and AGAMOUS. Cell 105(6):805–14.
Payne T., Johnson S.D. and Koltunow A.M. (2004) KNUCKLES (KNU) encodes a C2H2 zinc-finger protein that regulates development of basal pattern elements of the Arabidopsis gynoecium. Development 131(15):3737–49
Sun B., Xu Y., Ng K.H. and Ito T. (2009) A timing mechanism for stem cell maintenance and differentiation in the Arabidopsis floral meristem. Genes & Development 23(15):1791–804
Xu C., Liberatore K.L., MacAlister C.A., Huang Z., Chu Y.H., Jiang K., Brooks C., Ogawa-Ohnishi M., Xiong G., Pauly M. van Eck J., Matsubayashi Y., van der Knaap E. and Lippman Z.B. (2015) A cascade of arabinosyltransferases controls shoot meristem size in tomato. Nature Genetics 47, 784–792
