Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Arabidopsis thaliana constitutively active ROP11 interacts with the NADPH oxidase respiratory burst oxidase homologue F to regulate reactive oxygen species production in root hairs

Min Yan A , Wen Jing A , Ni Xu A , Like Shen A , Qun Zhang A B and Wenhua Zhang A B
+ Author Affiliations
- Author Affiliations

A College of Life Sciences, State Key Laboratory of Crop Genetics and Germplasm Enhancement, Nanjing Agricultural University, Nanjing 210095, P. R. China.

B Corresponding authors. Emails: zhangqun@njau.edu.cn; whzhang@njau.edu.cn

Functional Plant Biology 43(3) 221-231 https://doi.org/10.1071/FP15090
Submitted: 5 April 2015  Accepted: 12 November 2015   Published: 1 February 2016

Abstract

Reactive oxygen species (ROS) play a key signalling role in cells. Plant NADPH oxidases, also known as respiratory burst oxidase homologues (Rbohs), are well characterised ROS-generating systems. In this study, we found that the constitutively active small guanosine triphosphatase (GTPase) ROP11 (CA-ROP11) interacted with RbohF by using a yeast two-hybrid analysis, a pull-down assay and an in vivo bimolecular fluorescence complementation assay. The mutation of amino acid L336 or L337 in RbohF abolished its interaction with CA-ROP11. Coexpression of CA-ROP11 and wild-type RbohF in Nicotiana benthamiana Domin enhanced ROS production compared with coexpression of CA-ROP11 and mutant RbohF or of dominant negative ROP11 and wild-type RbohF. Moreover, CA-ROP11 overexpression resulted in ROS accumulation and a swollen root hair phenotype in Arabidopsis thaliana (L.) Heynh. The deletion of RbohF partially reduced the increase in ROS in Arabidopsis plants overexpressing CA-ROP11. These results suggest that Arabidopsis ROP11 modulates ROS production by interacting with RbohF in root hairs.

Additional keywords: coexpression, root hair.


References

Bloch D, Lavy M, Efrat Y, Efroni I, Bracha-Drori K, Abu-Abied M, Sadot E, Yalovsky S (2005) Ectopic expression of an activated RAC in Arabidopsis disrupts membrane cycling. Molecular Biology of the Cell 16, 1913–1927.
Ectopic expression of an activated RAC in Arabidopsis disrupts membrane cycling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjt1Kqtbw%3D&md5=9ccbcf1d994d55658c43fbbad951d200CAS | 15703216PubMed |

Bloch D, Monshausen G, Singer M, Gilroy S, Yalovsky S (2011) Nitrogen source interacts with ROP signalling in root hair tip-growth. Plant, Cell & Environment 34, 76–88.
Nitrogen source interacts with ROP signalling in root hair tip-growth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht1GnurY%3D&md5=9d6439efb9a71ba706e72491ecc2d608CAS |

Chen X, Naramoto S, Robert S, Tejos R, Löfke C, Lin D, Yang Z, Friml J (2012) ABP1 and ROP6 GTPase signaling regulate clathrin-mediated endocytosis in Arabidopsis roots. Current Biology 22, 1326–1332.
ABP1 and ROP6 GTPase signaling regulate clathrin-mediated endocytosis in Arabidopsis roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xot12ntrs%3D&md5=d543b59272f3bc5386f18404bf3e4fe6CAS | 22683261PubMed |

Drerup MM, Schlücking K, Hashimoto K, Manishankar P, Steinhorst L, Kuchitsu K, Kudla J (2013) The calcineurin B-like calcium sensors CBL1 and CBL9 together with their interacting protein kinase CIPK26 regulate the Arabidopsis NADPH oxidase RBOHF. Molecular Plant 6, 559–569.
The calcineurin B-like calcium sensors CBL1 and CBL9 together with their interacting protein kinase CIPK26 regulate the Arabidopsis NADPH oxidase RBOHF.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXksFWjtbc%3D&md5=4acc7a14039af63866ba3dd94dedfd6dCAS | 23335733PubMed |

Duan Q, Kita D, Li C, Cheung AY, Wu HM (2010) FERONIA receptor-like kinase regulates RHO GTPase signaling of root hair development. Proceedings of the National Academy of Sciences of the United States of America 107, 17821–17826.
FERONIA receptor-like kinase regulates RHO GTPase signaling of root hair development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlaltL7F&md5=5596e6ed89367d8578655028974e27d5CAS | 20876100PubMed |

Fehér A, Lajkó DB (2015) Signals fly when kinases meet Rho-of-plants (ROP) small G-proteins. Plant Science 237, 93–107.
Signals fly when kinases meet Rho-of-plants (ROP) small G-proteins.Crossref | GoogleScholarGoogle Scholar | 26089155PubMed |

Foreman J, Demidchik V, Bothwell JH, Mylona P, Miedema H, Torres MA, Linstead P, Costa S, Brownlee C, Jones JD, Davies JM, Dolan L (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422, 442–446.
Reactive oxygen species produced by NADPH oxidase regulate plant cell growth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXitlGgtLg%3D&md5=a7a4f2bcfd8ee509314e33a5040de58eCAS | 12660786PubMed |

Gu Y, Li S, Lord EM, Yang Z (2006) Members of a novel class of Arabidopsis Rho guanine nucleotide exchange factors control Rho GTPase-dependent polar growth. The Plant Cell 18, 366–381.
Members of a novel class of Arabidopsis Rho guanine nucleotide exchange factors control Rho GTPase-dependent polar growth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xhs1egu7g%3D&md5=0142a9cda7f646c89b3fe944b7f80f57CAS | 16415208PubMed |

Jiang M, Zhang J (2001) Effect of abscisic acid on active oxygen species, antioxidative defence system and oxidative damage in leaves of maize seedlings. Plant & Cell Physiology 42, 1265–1273.
Effect of abscisic acid on active oxygen species, antioxidative defence system and oxidative damage in leaves of maize seedlings.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXos1Oms74%3D&md5=e12987cb3d02744561af1eb4a04e9d9eCAS |

Jiao Y, Sun L, Song Y, Wang L, Liu L, Zhang L, Liu B, Li N, Miao C, Hao F (2013) AtrbohD and AtrbohF positively regulate abscisic acid-inhibited primary root growth by affecting Ca2+ signalling and auxin response of roots in Arabidopsis. Journal of Experimental Botany 64, 4183–4192.
AtrbohD and AtrbohF positively regulate abscisic acid-inhibited primary root growth by affecting Ca2+ signalling and auxin response of roots in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhs1ygs7vL&md5=7298eb91a23a8dcec9f8bc99fde53b56CAS | 23963673PubMed |

Jones MA, Raymond MJ, Yang Z, Smirnoff N (2007) NADPH oxidase-dependent reactive oxygen species formation required for root hair growth depends on ROP GTPase. Journal of Experimental Botany 58, 1261–1270.
NADPH oxidase-dependent reactive oxygen species formation required for root hair growth depends on ROP GTPase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXlvFGisrw%3D&md5=2eb2db45bad1ae3d189f1ab98104f3bfCAS | 17301029PubMed |

Keller T, Damude HG, Werner D, Doerner P, Dixon RA, Lamb C (1998) A plant homolog of the neutrophil NADPH oxidase gp91phox subunit gene encodes a plasma membrane protein with Ca2+ binding motifs. The Plant Cell 10, 255–266.

Kwak JM, Mori IC, Pei Z-M, Leonhardt N, Torres MA, Dangl JL, Bloom RE, Bodde S, Jones JD, Schroeder JI (2003) NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. The EMBO Journal 22, 2623–2633.
NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXkt1WrtLY%3D&md5=1b19593b0552608365fb26efced37abcCAS | 12773379PubMed |

Lavy M, Yalovsky S (2006) Association of Arabidopsis type-II ROPs with the plasma membrane requires a conserved C-terminal sequence motif and a proximal polybasic domain. The Plant Journal 46, 934–947.
Association of Arabidopsis type-II ROPs with the plasma membrane requires a conserved C-terminal sequence motif and a proximal polybasic domain.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XmvVWqtL8%3D&md5=204e65c86656499c5cad53657121b028CAS | 16805728PubMed |

Li Z, Liu D (2012) ROPGEF1 and ROPGEF4 are functional regulators of ROP11 GTPase in ABA-mediated stomatal closure in Arabidopsis. FEBS Letters 586, 1253–1258.
ROPGEF1 and ROPGEF4 are functional regulators of ROP11 GTPase in ABA-mediated stomatal closure in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xlt1ylt7o%3D&md5=e707f14da31dd4b7ef9d823629937c40CAS | 22500990PubMed |

Li Z, Kang J, Sui N, Liu D (2012a) ROP11 GTPase is a negative regulator of multiple ABA responses in Arabidopsis. Journal of Integrative Plant Biology 54, 169–179.
ROP11 GTPase is a negative regulator of multiple ABA responses in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XmslGjsLw%3D&md5=5bd1d007201c2815c9376591870e6175CAS | 22233300PubMed |

Li Z, Li Z, Gao X, Chinnusamy V, Bressan R, Wang ZX, Zhu JK, Wu JW, Liu D (2012b) ROP11 GTPase negatively regulates ABA signaling by protecting ABI1 phosphatase activity from inhibition by the ABA receptor RCAR1/PYL9 in Arabidopsis. Journal of Integrative Plant Biology 54, 180–188.
ROP11 GTPase negatively regulates ABA signaling by protecting ABI1 phosphatase activity from inhibition by the ABA receptor RCAR1/PYL9 in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XmslGjsL0%3D&md5=b12652a6f1b97d20fd593251aa32d307CAS | 22251383PubMed |

Li L, Li M, Yu L, Zhou Z, Liang X, Liu Z, Cai G, Gao L, Zhang X, Wang Y, Chen S, Zhou JM (2014) The FLS2-associated kinase BIK1 directly phosphorylates the NADPH oxidase RbohD to control plant immunity. Cell Host & Microbe 15, 329–338.
The FLS2-associated kinase BIK1 directly phosphorylates the NADPH oxidase RbohD to control plant immunity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXks1Onu70%3D&md5=b19b44b7a86ecd4a355005e9994d6de2CAS |

Li N, Sun L, Zhang L, Song Y, Hu P, Li C, Hao F (2015) AtrbohD and AtrbohF negatively regulate lateral root development by changing the localized accumulation of superoxide in primary roots of Arabidopsis. Planta 241, 591–602.
AtrbohD and AtrbohF negatively regulate lateral root development by changing the localized accumulation of superoxide in primary roots of Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhvFGjurvN&md5=20c23dc244b26e07fca6714f1b77ef71CAS | 25399352PubMed |

Marino D, Dunand C, Puppo A, Pauly N (2012) A burst of plant NADPH oxidases. Trends in Plant Science 17, 9–15.
A burst of plant NADPH oxidases.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XptVSnsQ%3D%3D&md5=b16499edc0fc4b8fc0ba8bdf6295b363CAS | 22037416PubMed |

Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiologia Plantarum 15, 473–497.
A revised medium for rapid growth and bio assays with tobacco tissue cultures.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF3sXksFKm&md5=3e14ca2e1300bcfb216c06e8c97b09daCAS |

Oda Y, Fukuda H (2012) Initiation of cell wall pattern by a Rho- and microtubule-driven symmetry breaking. Science 337, 1333–1336.
Initiation of cell wall pattern by a Rho- and microtubule-driven symmetry breaking.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtlaitL%2FP&md5=30bbdc71dbb65d67caac554dd9f797edCAS | 22984069PubMed |

Oda T, Hashimoto H, Kuwabara N, Akashi S, Hayashi K, Kojima C, Wong HL, Kawasaki T, Shimamoto K, Sato M (2010) Structure of the N-terminal regulatory domain of a plant NADPH oxidase and its functional implications. The Journal of Biological Chemistry 285, 1435–1445.
Structure of the N-terminal regulatory domain of a plant NADPH oxidase and its functional implications.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXkvFek&md5=8834cb3f178944273d3a0e52aa61394aCAS | 19864426PubMed |

Poraty-Gavra L, Zimmermann P, Haigis S, Bednarek P, Hazak O, Stelmakh OR, Sadot E, Schulze-Lefert P, Gruissem W, Yalovsky S (2013) The Arabidopsis Rho of plants GTPase AtROP6 functions in developmental and pathogen response pathways. Plant Physiology 161, 1172–1188.
The Arabidopsis Rho of plants GTPase AtROP6 functions in developmental and pathogen response pathways.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXmvFKrtb4%3D&md5=48c9f22f10a1d061b73c03af7cbe3f57CAS | 23319551PubMed |

Schnall JA, Quatrano RS (1992) Abscisic acid elicits the water-stress response in root hairs of Arabidopsis thaliana. Plant Physiology 100, 216–218.
Abscisic acid elicits the water-stress response in root hairs of Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XmtlSgtrg%3D&md5=323760d8b1e27e6bb6c7db2a0ca82a2aCAS | 16652949PubMed |

Sirichandra C, Gu D, Hu H-C, Davanture M, Lee S, Djaoui M, Valot B, Zivy M, Leung J, Merlot S (2009) Phosphorylation of the Arabidopsis AtrbohF NADPH oxidase by OST1 protein kinase. FEBS Letters 583, 2982–2986.
Phosphorylation of the Arabidopsis AtrbohF NADPH oxidase by OST1 protein kinase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFajsb3O&md5=8edccfd1aff7bdd498899f0821b065b4CAS | 19716822PubMed |

Suzuki N, Miller G, Morales J, Shulaev V, Torres MA, Mittler R (2011) Respiratory burst oxidases: the engines of ROS signaling. Current Opinion in Plant Biology 14, 691–699.
Respiratory burst oxidases: the engines of ROS signaling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsFygu7vJ&md5=eaa53f6eb5b6a9c40f3264cbb4efcab6CAS | 21862390PubMed |

Torres MA, Dangl JL (2005) Functions of the respiratory burst oxidase in biotic interactions, abiotic stress and development. Current Opinion in Plant Biology 8, 397–403.
Functions of the respiratory burst oxidase in biotic interactions, abiotic stress and development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXlsFGgtrg%3D&md5=1cef1b98bb4005ee8f81f7d8f501cdfeCAS | 15939662PubMed |

Torres MA, Onouchi H, Hamada S, Machida C, Hammond-Kosack KE, Jones JD (1998) Six Arabidopsis thaliana homologues of the human respiratory burst oxidase (gp91phox ). The Plant Journal 14, 365–370.
Six Arabidopsis thaliana homologues of the human respiratory burst oxidase (gp91phox ).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXjslOlsr0%3D&md5=fc7452d41ca6b1ef0441f3381034356aCAS | 9628030PubMed |

Torres MA, Dangl JL, Jones JD (2002) Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proceedings of the National Academy of Sciences of the United States of America 99, 517–522.
Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xlt1CqsQ%3D%3D&md5=59c35b06495f04502c176a2b28154f05CAS | 11756663PubMed |

Wong HL, Pinontoan R, Hayashi K, Tabata R, Yaeno T, Hasegawa K, Kojima C, Yoshioka H, Iba K, Kawasaki T (2007) Regulation of rice NADPH oxidase by binding of Rac GTPase to its N-terminal extension. The Plant Cell 19, 4022–4034.
Regulation of rice NADPH oxidase by binding of Rac GTPase to its N-terminal extension.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhvF2ht7Y%3D&md5=aca6d12a7c8b802b4a13efe276fb7160CAS | 18156215PubMed |

Yu F, Qian L, Nibau C, Duan Q, Kita D, Levasseur K, Li X, Lu C, Li H, Hou C, Li L, Buchanan BB, Chen L, Cheung AY, Li D, Luan S (2012) FERONIA receptor kinase pathway suppresses abscisic acid signaling in Arabidopsis by activating ABI2 phosphatase. Proceedings of the National Academy of Sciences of the United States of America 109, 14693–14698.
FERONIA receptor kinase pathway suppresses abscisic acid signaling in Arabidopsis by activating ABI2 phosphatase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsVaqu73F&md5=39110cfc1489898178a0948d321a5809CAS | 22908257PubMed |

Zhang Y, Zhu H, Zhang Q, Li M, Yan M, Wang R, Wang L, Welti R, Zhang W, Wang X (2009) Phospholipase Dα1 and phosphatidic acid regulate NADPH oxidase activity and production of reactive oxygen species in ABA-mediated stomatal closure in Arabidopsis. The Plant Cell 21, 2357–2377.
Phospholipase Dα1 and phosphatidic acid regulate NADPH oxidase activity and production of reactive oxygen species in ABA-mediated stomatal closure in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXht12qsLrI&md5=dbb47020ba667190bfe67fc804812e4fCAS | 19690149PubMed |

Zhao R, Sun HL, Mei C, Wang XJ, Yan L, Liu R, Zhang XF, Wang XF, Zhang DP (2011) The Arabidopsis Ca2+-dependent protein kinase CPK12 negatively regulates abscisic acid signaling in seed germination and post-germination growth. New Phytologist 192, 61–73.
The Arabidopsis Ca2+-dependent protein kinase CPK12 negatively regulates abscisic acid signaling in seed germination and post-germination growth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht12jt7nL&md5=6210d4c3412adb1f9b0bc733738833ebCAS | 21692804PubMed |

Zheng ZL, Yang Z (2000) The Rop GTPase: an emerging signaling switch in plants. Plant Molecular Biology 44, 1–9.
The Rop GTPase: an emerging signaling switch in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXotlaju74%3D&md5=202f1b7980cd106857f604235d140e2dCAS | 11094975PubMed |