Functionally redundant LNG3 and LNG4 genes regulate turgor-driven polar cell elongation through activation of XTH17 and XTH24

Abstract

In this work, we genetically characterized the function of Arabidopsis thaliana, LONGIFOLIA (LNG1), LNG2, LNG3, LNG4, their contribution to regulate vegetative architecture in plant. We used molecular and biophysical approaches to elucidate a gene function that regulates vegetative architecture, as revealed by the leaf phenotype and later effects on flowering patterns in Arabidopsis loss-of-function mutants. As a result, LNG genes play an important role in polar cell elongation by turgor pressure controlling the activation of XTH17 and XTH24. Plant vegetative architecture is related to important traits that later influence the floral architecture involved in seed production. Leaf morphology is the primary key trait to compose plant vegetative architecture. However, molecular mechanism on leaf shape determination is not fully understood even in the model plant A. thaliana. We previously showed that LONGIFOLIA (LNG1) and LONGIFOLIA2 (LNG2) genes regulate leaf morphology by promoting longitudinal cell elongation in Arabidopsis. In this study, we further characterized two homologs of LNG1, LNG3, and LNG4, using genetic, biophysical, and molecular approaches. Single loss-of-function mutants, lng3 and lng4, do not show any phenotypic difference, but mutants of lng quadruple (lngq), and lng1/2/3 and lng1/2/4 triples, display reduced leaf length, compared to wild type. Using the paradermal analysis, we conclude that the reduced leaf size of lngq is due to decreased cell elongation in the direction of longitudinal leaf growth, and not decreased cell proliferation. This data indicate that LNG1/2/3/4 are functionally redundant, and are involved in polar cell elongation in Arabidopsis leaf. Using a biophysical approach, we show that the LNGs contribute to maintain high turgor pressure, thus regulating turgor pressure-dependent polar cell elongation. In addition, gene expression analysis showed that LNGs positively regulate the expression of the cell wall modifying enzyme encoded by a multi-gene family, xyloglucan endotransglucosylase/hydrolase (XTH). Taking all of these together, we propose that LNG related genes play an important role in polar cell elongation by changing turgor pressure and controlling the activation of XTH17 and XTH24.

EST–SNP Study of Olea europaea L. Uncovers Functional Polymorphisms between Cultivated and Wild Olives

“…The LFY promoter contains binding sites for several regulatory factors like Agamous-like MADS-box (AGL) [85], and in Citrus, the constitutive expression of LFY was found to reduce the juvenile phase [86]. An nsSNP was found between wild and cultivated olives in the XTH9 gene, whose expression was reduced in various mutants that had a defect in elongation, including acaulis pin-formed and terminal flower [87]. Moreover, under stress conditions, specific XTH isoforms were up-regulated, while others were down-regulated, suggesting a different involvement of the XTH enzymes on the effects of simultaneous exposure to dehydration and heat conditions, naturally occurring in open fields [88].…”

Auxin promotion of seedling growth via ARF5 is dependent on the brassinosteroid‐regulated transcription factors BES1 and BEH4

“…Overexpression of XTH18, XTH19, and XTH20 (all part of the bipartite XTH clade) stimulated hypocotyl growth in early developmental stage of Arabidopsis seedlings (Miedes et al, ), while similarly loss of function of XTH17 results in inhibition of hypocotyl growth (Figure d). In addition, the functionally redundant LNG3 and LNG4 genes regulate turgor‐driven polar cell elongation through activation of XTH17 and XTH24 (Lee et al, ). BES1/BZR1 and PIFs were also implicated in hypocotyl elongation during thermomorphogenesis via regulation of LNG1 and LNG2 (Hwang et al, ; Ibañez et al, ; Li et al, ).…”

Mechanisms underlying the enhanced biomass and abiotic stress tolerance phenotype of an Arabidopsis MIOX over‐expresser

“…Interestingly, A. thaliana arabinogalactan protein (AtAGP17) over-expression results in resistance to infection by Agrobacterium (Gaspar et al, 2004). The expression of the gene longofolia is involved in polar cell expansion by turgor-driven approach by controlling XTH17 and XTH24 expression (Lee et al, 2018). In contrast, CSLA/CSLA-like gene family members that are involved in mannan and xyloglucan backbones biosynthesis (Liepman & Cavalier, 2012) were up-regulated in AtMIOX4 OE line compared to the WT control.…”