Research Article: Heterogeneity in the expression and subcellular localization of POLYOL/MONOSACCHARIDE TRANSPORTER genes in Lotus japonicus

Date Published: September 20, 2017

Publisher: Public Library of Science

Author(s): Lu Tian, Leru Liu, Yehu Yin, Mingchao Huang, Yanbo Chen, Xinlan Xu, Pingzhi Wu, Meiru Li, Guojiang Wu, Huawu Jiang, Yaping Chen, Hernâni Gerós.

http://doi.org/10.1371/journal.pone.0185269

Abstract

Polyols can serve as a means for the translocation of carbon skeletons and energy between source and sink organs as well as being osmoprotective solutes and antioxidants which may be involved in the resistance of some plants to biotic and abiotic stresses. Polyol/Monosaccharide transporter (PLT) proteins previously identified in plants are involved in the loading of polyols into the phloem and are reported to be located in the plasma membrane. The functions of PLT proteins in leguminous plants are not yet clear. In this study, a total of 14 putative PLT genes (LjPLT1-14) were identified in the genome of Lotus japonicus and divided into 4 clades based on phylogenetic analysis. Different patterns of expression of LjPLT genes in various tissues were validated by qRT-PCR analysis. Four genes (LjPLT3, 4, 11, and 14) from clade II were expressed at much higher levels in nodule than in other tissues. Moreover, three of these genes (LjPLT3, 4, and 14) showed significantly increased expression in roots after inoculation with Mesorhizobium loti. Three genes (LjPLT1, 3, and 9) responded when salinity and/or osmotic stresses were applied to L. japonicus. Transient expression of GFP-LjPLT fusion constructs in Arabidopsis and Nicotiana benthamiana protoplasts indicated that the LjPLT1, LjPLT6 and LjPLT7 proteins are localized to the plasma membrane, but LjPLT2 (clade IV), LjPLT3, 4, 5 (clade II) and LjPLT8 (clade III) proteins possibly reside in the Golgi apparatus. The results suggest that members of the LjPLT gene family may be involved in different biological processes, several of which may potentially play roles in nodulation in this nitrogen-fixing legume.

Partial Text

Polyols are a reduced form of aldose and ketose sugars. The carbon chain of polyols can be either linear (acyclic polyols) or cyclic (arranged in a ring). Within the higher plants, at least 13 different polyols have been identified in angiosperms [1]. In some plants, such as woody Rosaceae and celery (Apium graveolens L. var. dulce), polyols (mainly sorbitol or mannitol) are, together with sucrose, direct products of photosynthetic carbon fixation. In these species, polyols can perform functions similar to those of sucrose, such as the translocation of carbon skeletons and transfer of energy between sources and sink organs [2–4]. Plant polyols can also function as osmoprotective solutes and antioxidants which may be involved in biotic [5, 6] and abiotic stress tolerance [7–10].

In the present study, a total of 14 PLT genes were identified in the L. japonicus genome. The LjPLT proteins could be divided into 4 clades according to the results of phylogenetic analysis (Fig 2 and S1 Fig). Hydropathy analyses of the protein sequences showed that LjPLTs have 6 + 6 transmembrane domains (Fig 1). Gene duplication has occurred throughout plant evolution, contributing to the establishment of new gene functions and underlying the origins of evolutionary novelty [30, 39]. In apple, MdSOT3, MdSOT4, and MdSOT5 from source leaves are more closely related to polyol transporter homologs from Rosaceae than to those from other families. This suggests that the Rosaceae sorbitol transporter homologs diverged after the Rosaceae had evolved away from other families [15]. Similarly, in L. japonicus three PLT genes in clade I and three in clade III may have originated from gene duplication events and diverged after the Leguminosae had evolved from other families. Most of the L. japonicus PLT genes fell into clade II (Fig 2 and S1 Fig). Two tandem arrays of clade II genes were identified (S2 Table), one of which was also detected in the genomes of other Leguminosae species such as G. max and P. vulgaris (S1 Fig). LjPLT3, 4, and 5, which are located in a tandem repeat region on chromosome 2, fell into subclade IIa (LjPLT3 and 4) and subclade IIb (LjPLT5) (S1 Fig). This tandem duplication and divergence of genes were also observed in the genomes of G. max and P. vulgaris (S1 Fig and S3 Table). These results suggested that the expansion of the PLT gene family in L. japonicus resulted from duplication events that occurred both before and after the separation of the Leguminosae family.

 

Source:

http://doi.org/10.1371/journal.pone.0185269