Heterochrony of plant meristem: unusual organogenesis of Monophyllaea

We discovered a unique plant meristem that seems to be evolved by neoteny of the shoot apical meristem from studies of one-leaf plant, Monophyllaea.
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We are pursuing developmental genetics and evolutionary developmental biology on leaves using Arabidopsis as a model species and the other so-called non-model plant species in The University of Tokyo, Japan.  The latter include genus Monophyllaea (Gesneriaceae, Figure 1) that is unique in having indeterminately growing cotyledon without making foliage leaves during the vegetative phase. As the genus name indicates, Monophyllaea species appear to have only one indeterminate leaf when it flowers, so they have a name ‘one-leaf plants’. We started studies on Monophyllaea in late 1990s and published one report on the competitive nature for fate determination of the cotyledons, but due to the difficulties in studying non-model species from molecular genetics, our studies have paused until recently.

Figure 1
Fig. 1 Unique body plan of Monophyllaea. All members of this genus appear to have only one, indeterminately growing leaf at anthesis, that is derived from one of two cotyledons. 

But nowadays many novel techniques have been developed to overcome the obstacles in molecular studies of non-model species. For instance, high-throughput sequencing reveals genomic and transcriptomic perspectives and accelerates the application of established methods, such as in situ hybridization, to novel plant materials.

We previously succeeded in introducing whole-mount in situ hybridization technique to seedlings of Monophyllaea associated with RNAseq with gene annotation and found several curious natures in the meristematic region of the indeterminately growing cotyledon. The first discovery from our new studies was the co-expression of class I KNOX gene that is usually expressed specifically in the shoot apical meristem and ANGUSTIFOLIA3 gene that is usually expressed in the leaf meristem. Is not shoot apical meristem and leaf meristem precisely differentiated in Monophyllaea meristem?

Recently, we examined whether the boundary gene, CUP-SHAPED COTYLEDON, which is usually expressed in the border region between the shoot apical meristem and leaf primordia, is correctly expressed around the meristem or not. As a result, we surprisingly found that the CUP-SHAPED COTYLEDON gene is co-expressed with the class I KNOX gene in the Monophyllaea vegetative meristem (Fig. 2). Interestingly, in the model plant, Arabidopsis, such co-expression is seen only transiently in the very early stage of the shoot apical meristem initiation in young embryo. From this discovery, we proposed that the vegetative meristem of Monophyllaea remains in the earliest stage of juvenile shoot apical meristem. In other words, the unique Monophyllaea vegetative meristem would be evolved by neoteny of the shoot apical meristem.

Fig. 2
Fig. 2 Schematic figure that shows unique expression pattern of the CUP-SHAPED COTYLEDON (CUC) gene and the class I KNOX gene (STM). Drawing Dr. Shuji Nakamura, The Univ. Tokyo).aption

We think this discovery will be a good basis for further investigation of the Monophyllaea meristem. Because, to date, no Arabidopsis mutant shows indeterminacy in the leaf primordia, Monophyllaea is the best material as a natural mutant to pursue how leaf meristem of usual plants has a determinate fate. We are now adopting the single-nucleus RNAseq technique to the Monophyllaea meristem to get more clues to understand the molecular nature of the meristem, which will result in the next series of publications.

Our research is published in Scientific Reports Special Issue—Plant Stem Cell—organized by Editor Prof. Chunli Chen, Dr. Wouter Kohlen, and Dr. Nobutoshi Yamaguchi. If you want to read our work, follow the link:

https://rdcu.be/dH03O

Please feel free to contact me at tsukaya@bs.s.u-tokyo.ac.jp if you have any questions or comments about the work.

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Plant Development
Life Sciences > Biological Sciences > Plant Science > Plant Development
Evolutionary Developmental Biology
Life Sciences > Biological Sciences > Evolutionary Biology > Evolutionary Developmental Biology

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