Loss or duplication of key regulatory genes coincides with environmental adaptation of the stomatal complex in Nymphaea colorata and Kalanchoe laxiflora

Meizhi Xu,Fei Chen,Shuang Wu,Shilian Qi,Liangsheng Zhang

doi:10.1038/s41438-018-0048-8

Meizhi Xu, Fei Chen + Show 3 more

Open Access

https://doi.org/10.1038/s41438-018-0048-8

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Abstract

The stomatal complex is critical for gas and water exchange between plants and the atmosphere. Originating over 400 million years ago, the structure of the stomata has evolved to facilitate the adaptation of plants to various environments. Although the molecular mechanism of stomatal development in Arabidopsis has been widely studied, the evolution of stomatal structure and its molecular regulators in different species remains to be answered. In this study, we examined stomatal development and the orthologues of Arabidopsis stomatal genes in a basal angiosperm plant, Nymphaea colorata, and a member of the eudicot CAM family, Kalanchoe laxiflora, which represent the adaptation to aquatic and drought environments, respectively. Our results showed that despite the conservation of core stomatal regulators, a number of critical genes were lost in the N. colorata genome, including EPF2, MPK6, and AP2C3 and the polarity regulators BASL and POLAR. Interestingly, this is coincident with the loss of asymmetric divisions during the stomatal development of N. colorata. In addition, we found that the guard cell in K. laxiflora is surrounded by three or four small subsidiary cells in adaxial leaf surfaces. This type of stomatal complex is formed via repeated asymmetric cell divisions and cell state transitions. This may result from the doubled or quadrupled key genes controlling stomatal development in K. laxiflora. Our results show that loss or duplication of key regulatory genes is associated with environmental adaptation of the stomatal complex.

Highlights

Stomata are a pore-like structure in multiple organs, including leaves and stems, which facilitates gas and water exchange
Loss of stomatal development genes in N. colorata It was reported that different stomatal development patterns occur in plants of the ANITA grade
On the abaxial surface of N. colorata, we only found hydropote complexes with lens-shaped cells and bowl-shaped cells, which appeared to be surrounded by specialized rosettes of epidermal cells (Fig. 1b)

Summary

Introduction

Stomata are a pore-like structure in multiple organs, including leaves and stems, which facilitates gas and water exchange. When environmental conditions are unfavourable, plants can regulate water evapotranspiration and reduce CO2 uptake by opening and closing the stomata. Crassulacean acid metabolism (CAM) plants are adapted to arid conditions[1]. The stomata in CAM plants remain closed during the day to reduce evapotranspiration while staying open at night to absorb. These physiological traits make CAM plants resistant to diverse stresses, including strong irradiance and drought[2]. Stomatal structure is highly conserved across land plants. The patterning of the mature stomatal structure differs among plant groups and can be generally summarized by three classes: anomocytic, stephanocytic, and paracytic[4].

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