TY - JOUR
T1 - Root-tip-mediated inhibition of hydrotropism is accompanied with the suppression of asymmetric expression of auxin-inducible genes in response to moisture gradients in cucumber roots
AU - Fujii, Nobuharu
AU - Miyabayashi, Sachiko
AU - Sugita, Tomoki
AU - Kobayashi, Akie
AU - Yamazaki, Chiaki
AU - Miyazawa, Yutaka
AU - Kamada, Motoshi
AU - Kasahara, Haruo
AU - Osada, Ikuko
AU - Shimazu, Toru
AU - Fusejima, Yasuo
AU - Higashibata, Akira
AU - Yamazaki, Takashi
AU - Ishioka, Noriaki
AU - Takahashi, Hideyuki
N1 - Funding Information:
This study was conducted by the Ground-Based Research Announcement for Space Utilization program promoted by the Japan Space Forum. This work also was supported by a Grant-in-Aid for Scientific Research on Innovative Areas (no. 24620002) from the Ministry of Education, Culture, Sports, Science, and Technology (MEXT) of Japan to H.T., by a Grant-in-Aid for Scientific Research (C) (no. 16K07955) from the Japan Society for the Promotion of Science (JSPS) to H. T., by a Grant-in-Aid for Young Scientists (B) (no. 26870057) from the JSPS to A.K., by the Funding Program for Next-Generation World-Leading Researchers (GS002) from the Council for Science and Technology Policy, Cabinet Office, and JSPS to Y.M., and by a Grant-in-Aid for Scientific Research (C) (K15K119130) from the JSPS to N.F. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Motoshi Kamada is employed by Advanced Engineering Services Co., Ltd. Ikuko Osada is employed by Japan Manned Space Systems Co., Ltd. Advanced Engineering Services Co., Ltd. and Japan Manned Space Systems Co., Ltd. provided support in the form of salaries for authors M.K. and I.O., but did not have any additional role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript. The specific roles of these authors are articulated in the “author contributions” section. We are grateful to MEXT KAKENHI (no. 221S0002) for supporting the RNA-Seq analysis of cucumber root gravitropism in this work.
Publisher Copyright:
© 2018 Fujii et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
PY - 2018/1
Y1 - 2018/1
N2 - In cucumber seedlings, gravitropism interferes with hydrotropism, which results in the nearly complete inhibition of hydrotropism under stationary conditions. However, hydrotropic responses are induced when the gravitropic response in the root is nullified by clinorotation. Columella cells in the root cap sense gravity, which induces the gravitropic response. In this study, we found that removing the root tip induced hydrotropism in cucumber roots under stationary conditions. The application of auxin transport inhibitors to cucumber seedlings under stationary conditions suppressed the hydrotropic response induced by the removal of the root tip. To investigate the expression of genes related to hydrotropism in de-tipped cucumber roots, we conducted transcriptome analysis of gene expression by RNA-Seq using seedlings exhibiting hydrotropic and gravitropic responses. Of the 21 and 45 genes asymmetrically expressed during hydrotropic and gravitropic responses, respectively, five genes were identical. Gene ontology (GO) analysis indicated that the category auxin-inducible genes was significantly enriched among genes that were more highly expressed in the concave side of the root than the convex side during hydrotropic or gravitropic responses. Reverse transcription followed by quantitative polymerase chain reaction (RT-qPCR) analysis revealed that root hydrotropism induced under stationary conditions (by removing the root tip) was accompanied by the asymmetric expression of several auxin-inducible genes. However, intact roots did not exhibit the asymmetric expression patterns of auxin-inducible genes under stationary conditions, even in the presence of a moisture gradient. These results suggest that the root tip inhibits hydrotropism by suppressing the induction of asymmetric auxin distribution. Auxin transport and distribution not mediated by the root tip might play a role in hydrotropism in cucumber roots.
AB - In cucumber seedlings, gravitropism interferes with hydrotropism, which results in the nearly complete inhibition of hydrotropism under stationary conditions. However, hydrotropic responses are induced when the gravitropic response in the root is nullified by clinorotation. Columella cells in the root cap sense gravity, which induces the gravitropic response. In this study, we found that removing the root tip induced hydrotropism in cucumber roots under stationary conditions. The application of auxin transport inhibitors to cucumber seedlings under stationary conditions suppressed the hydrotropic response induced by the removal of the root tip. To investigate the expression of genes related to hydrotropism in de-tipped cucumber roots, we conducted transcriptome analysis of gene expression by RNA-Seq using seedlings exhibiting hydrotropic and gravitropic responses. Of the 21 and 45 genes asymmetrically expressed during hydrotropic and gravitropic responses, respectively, five genes were identical. Gene ontology (GO) analysis indicated that the category auxin-inducible genes was significantly enriched among genes that were more highly expressed in the concave side of the root than the convex side during hydrotropic or gravitropic responses. Reverse transcription followed by quantitative polymerase chain reaction (RT-qPCR) analysis revealed that root hydrotropism induced under stationary conditions (by removing the root tip) was accompanied by the asymmetric expression of several auxin-inducible genes. However, intact roots did not exhibit the asymmetric expression patterns of auxin-inducible genes under stationary conditions, even in the presence of a moisture gradient. These results suggest that the root tip inhibits hydrotropism by suppressing the induction of asymmetric auxin distribution. Auxin transport and distribution not mediated by the root tip might play a role in hydrotropism in cucumber roots.
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U2 - 10.1371/journal.pone.0189827
DO - 10.1371/journal.pone.0189827
M3 - Article
C2 - 29324818
AN - SCOPUS:85040378841
SN - 1932-6203
VL - 13
JO - PLoS ONE
JF - PLoS ONE
IS - 1
M1 - e0189827
ER -