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

PLDα1 and GPA1 are involved in the stomatal closure induced by Oridonin in Arabidopsis thaliana

Yue Zhang A , Ruirui Liu A , Yaping Zhou A , Simin Wang A , Bianfeng Zhang A , Juantao Kong A , Sheng Zheng A and Ning Yang https://orcid.org/0000-0003-1841-8010 A B
+ Author Affiliations
- Author Affiliations

A College of Life Sciences, Northwest Normal University, Lanzhou 730070, People’s Republic of China.

B Corresponding author. Email: xbsd-yn@163.com

Functional Plant Biology 48(10) 1005-1016 https://doi.org/10.1071/FP21156
Submitted: 17 May 2021  Accepted: 3 June 2021   Published: 25 June 2021

Abstract

Oridonin is an important diterpenoid, which plays an important role in plant growth and development. PLDα1 and GPA1 are involved in many biotic or abiotic stresses. In this study, using the seedlings of Arabidopsis thaliana L. wild type (WT), PLDα1 defective mutant (pldα1), GPA1 defective mutant (gpa1) and pldα1/gpa1 double mutant as materials, the effect of stomatal apertures responding to Oridonin and the functions of PLDα1 and GPA1 in this response were investigated. The results showed that 60 μmol·L–1 of Oridonin induced stomatal closure and significantly increased the relative expression levels of GPA1 and PLDα1. Oridonin increased H2O2 accumulation in guard cells by inhibiting the antioxidant enzymes. The increase of H2O2 caused the expression of OST1, which is a positive regulatory gene for stomatal closure. Both PLDα1 and GPA1 were involved in Oridonin-induced stomatal closure and PLDα1 acted downstream of GPA1. The results suggested that Oridonin caused stomatal closure by affecting GPA1 and promoting PLDα1 to produce PA, and further accumulating H2O2 to upregulate gene OST1.

Keywords: Oridonin, phospholipase Dα1, GPA1, hydrogen peroxide, stomatal closure, Arabidopsis thaliana L.


References

Bakhshayeshan-Agdam H, Lisar SYS, Motafakkerazad R (2019) Allelopathic effects of redroot pigweed (Amaranthus retroflexus L.) aqueous extract on cucumber and wheat. Allelopathy Journal 46, 55–72.
Allelopathic effects of redroot pigweed (Amaranthus retroflexus L.) aqueous extract on cucumber and wheat.Crossref | GoogleScholarGoogle Scholar |

Bright J, Desikan R, Hancock JT, Weir IS, Neill SJ (2006) ABA‐induced NO generation and stomatal closure in Arabidopsis are dependent on H2O2 synthesis. The Plant Journal 45, 113–122.
ABA‐induced NO generation and stomatal closure in Arabidopsis are dependent on H2O2 synthesis.Crossref | GoogleScholarGoogle Scholar | 16367958PubMed |

Cheng W, Zhang L, Jiao C, Su M, Yang T, Zhou L, Peng RY, Wang RR, Wang CY (2013) Hydrogen sulfide alleviates hypoxia-induced root tip death in Pisum sativum. Plant Physiology and Biochemistry 70, 278–286.
Hydrogen sulfide alleviates hypoxia-induced root tip death in Pisum sativum.Crossref | GoogleScholarGoogle Scholar | 23800663PubMed |

Chiang CM, Chen SP (2014) Expression of the broccoli catalase gene (BoCAT) enhances heat tolerance in transgenic Arabidopsis. Journal of Plant Biochemistry and Biotechnology 23, 266–277.
Expression of the broccoli catalase gene (BoCAT) enhances heat tolerance in transgenic Arabidopsis.Crossref | GoogleScholarGoogle Scholar |

Choudhury SR, Pandey S (2016) The role of PLDα1 in providing specificity to signal‐response coupling by heterotrimeric G‐protein components in Arabidopsis. The Plant Journal 86, 50–61.
The role of PLDα1 in providing specificity to signal‐response coupling by heterotrimeric G‐protein components in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |

Ding H, Ahmad A, Cheng Z (2020) An allelopathic role for garlic root exudates in the regulation of carbohydrate metabolism in cucumber in a hydroponic co-culture system. Plants 9, 45
An allelopathic role for garlic root exudates in the regulation of carbohydrate metabolism in cucumber in a hydroponic co-culture system.Crossref | GoogleScholarGoogle Scholar |

Guo L, Mishra G, Markham JE, Li MY, Tawfall A, Welti R, Wang XM (2012) Connections between sphingosine kinase and phospholipase D in the abscisic acid signaling pathway in Arabidopsis. The Journal of Biological Chemistry 287, 8286–8296.
Connections between sphingosine kinase and phospholipase D in the abscisic acid signaling pathway in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 22275366PubMed |

He H, Yan JW, Yu XY, Liang Y, Fang L, Henrik VS, Zhang A (2017) The NADPH-oxidase AtRbohI plays a positive role in drought-stress response in Arabidopsis thaliana. Biochemical and Biophysical Research Communications 491, 834–839.
The NADPH-oxidase AtRbohI plays a positive role in drought-stress response in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 28559135PubMed |

Hong Y, Zhang W, Wang X (2010) Phospholipase D and phosphatidic acid signalling in plant response to drought and salinity. Plant, Cell & Environment 33, 627–635.
Phospholipase D and phosphatidic acid signalling in plant response to drought and salinity.Crossref | GoogleScholarGoogle Scholar |

Huang Y, Bai Y, Wang Y, Kong H (2013) Allelopathic effects of the extracts from an invasive species S olidago canadensis L. on Microcystis aeruginosa. Letters in Applied Microbiology 57, 451–458.
Allelopathic effects of the extracts from an invasive species S olidago canadensis L. on Microcystis aeruginosa.Crossref | GoogleScholarGoogle Scholar | 23848059PubMed |

Islam MM, Munemasa S, Hossain MA, Nakamura Y, Mori IC, Murata Y (2010) Roles of AtTPC1, vacuolar two pore channel 1, in Arabidopsis stomatal closure. Plant & Cell Physiology 51, 302–311.
Roles of AtTPC1, vacuolar two pore channel 1, in Arabidopsis stomatal closure.Crossref | GoogleScholarGoogle Scholar |

Jahan MS, Ogawa KI, Nakamura Y, Shimoishi Y, Mori IC, Murata Y (2008) Deficient glutathione in guard cells facilitates abscisic acid-induced stomatal closure but does not affect light-induced stomatal opening. Bioscience, Biotechnology, and Biochemistry 72, 2795–2798.
Deficient glutathione in guard cells facilitates abscisic acid-induced stomatal closure but does not affect light-induced stomatal opening.Crossref | GoogleScholarGoogle Scholar | 18838781PubMed |

Jha Y, Subramanian RB (2014) PGPR regulate caspase-like activity, programmed cell death, and antioxidant enzyme activity in paddy under salinity. Physiology and Molecular Biology of Plants 20, 201–207.
PGPR regulate caspase-like activity, programmed cell death, and antioxidant enzyme activity in paddy under salinity.Crossref | GoogleScholarGoogle Scholar | 24757324PubMed |

Jiao CJ, Jiang JL, Li C, Ke LM, Cheng W, Li FM, Li ZX, Wang CY (2011) β-ODAP accumulation could be related to low levels of superoxide anion and hydrogen peroxide in Lathyrus sativus L. Food and Chemical Toxicology 49, 556–562.
β-ODAP accumulation could be related to low levels of superoxide anion and hydrogen peroxide in Lathyrus sativus L.Crossref | GoogleScholarGoogle Scholar | 20510333PubMed |

Jin X, Wang RS, Zhu M, Jeon BW, Albert R, Chen S, Assmann SM (2013) Abscisic acid–responsive guard cell metabolomes of Arabidopsis wild-type and gpa1 G-protein mutants. The Plant Cell 25, 4789–4811.
Abscisic acid–responsive guard cell metabolomes of Arabidopsis wild-type and gpa1 G-protein mutants.Crossref | GoogleScholarGoogle Scholar | 24368793PubMed |

Khokon MAR, Okuma E, Hossain MA, Munemasa S, Uraji M, Nakamura Y, Mori IC, Murata Y (2011) Involvement of extracellular oxidative burst in salicylic acid‐induced stomatal closure in Arabidopsis. Plant, Cell & Environment 34, 434–443.
Involvement of extracellular oxidative burst in salicylic acid‐induced stomatal closure in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |

Kumar AS, Bais HPK (2010) Allelopathy and exotic plant invasion. Plant Communication from an Ecological Perspective. 4, 61–74.
Allelopathy and exotic plant invasion.Crossref | GoogleScholarGoogle Scholar |

Lazzarino G, Tavazzi B, Pierro DD, Vagnozzi R, Penco M, Giardina B (1995) The relevance of malondialdehyde as a biochemical index of lipid peroxidation of postischemic tissues in the rat and human beings. Biological Trace Element Research 47, 165–170.
The relevance of malondialdehyde as a biochemical index of lipid peroxidation of postischemic tissues in the rat and human beings.Crossref | GoogleScholarGoogle Scholar | 7779543PubMed |

Li J, Zhang WH (2009) PLDα1 modulated ABA-mediated main root elongation and regulated tip growth of root hair in Arabidopsis. Yunnan Zhi Wu Yan Jiu 31, 309–316.
PLDα1 modulated ABA-mediated main root elongation and regulated tip growth of root hair in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |

Li JH, Liu YQ, Lü P, Lin HF, Bai Y, Wang XC, Chen YL (2009) A signaling pathway linking nitric oxide production to heterotrimeric G protein and hydrogen peroxide regulates extracellular calmodulin induction of stomatal closure in Arabidopsis. Plant Physiology 150, 114–124.
A signaling pathway linking nitric oxide production to heterotrimeric G protein and hydrogen peroxide regulates extracellular calmodulin induction of stomatal closure in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 19321706PubMed |

Li L, Zhang Y, Ding Y, Zhang YJ, Wang CQ, Liu Q (2012) Effects of Casuarina equisetifolia leachates on photosynthesis of Vatica mangachapoi Blanco seedlings. Allelopathy Journal 29, 231–240.

Li Y, Xu SS, Gao J, Pan S, Wang GX (2014) Chlorella triggers stomatal closure mediated by NADPH oxidase and improves instantaneous water use efficiency in Vicia faba. Plant Signaling & Behavior 9, e29078
Chlorella triggers stomatal closure mediated by NADPH oxidase and improves instantaneous water use efficiency in Vicia faba.Crossref | GoogleScholarGoogle Scholar |

Lin KH, Sei SC, Su YH, Chiang CM (2019) Overexpression of the Arabidopsis and winter squash superoxide dismutase genes enhances chilling tolerance via ABA-sensitive transcriptional regulation in transgenic Arabidopsis. Plant Signaling & Behavior 14, 1685728
Overexpression of the Arabidopsis and winter squash superoxide dismutase genes enhances chilling tolerance via ABA-sensitive transcriptional regulation in transgenic Arabidopsis.Crossref | GoogleScholarGoogle Scholar |

Liu G, Ding L, Yang Y, Yang H, Yang QM, Wang HQ (2006) Anti-oxidative action of ent-kaurene diterpenoids. Research on Chemical Intermediates 32, 787–794.
Anti-oxidative action of ent-kaurene diterpenoids.Crossref | GoogleScholarGoogle Scholar |

Liu F, Bian Z, Jia ZH, Zhao Q, Song SS (2012) The GCR1 and GPA1 participate in promotion of Arabidopsis primary root elongation induced by N-acyl-homoserine lactones, the bacterial quorum-sensing signals. Molecular Plant-Microbe Interactions 25, 677–683.
The GCR1 and GPA1 participate in promotion of Arabidopsis primary root elongation induced by N-acyl-homoserine lactones, the bacterial quorum-sensing signals.Crossref | GoogleScholarGoogle Scholar | 22250582PubMed |

Liu J, Sun X, Xu F, Zhang Y, Zhang Q, Miao R, Zhang J, Liang J, Xu W (2018) Suppression of OsMDHAR4 enhances heat tolerance by mediating H2O2-induced stomatal closure in rice plants. Rice (New York, N.Y.) 11, 38
Suppression of OsMDHAR4 enhances heat tolerance by mediating H2O2-induced stomatal closure in rice plants.Crossref | GoogleScholarGoogle Scholar |

Ma Y, Niu J (2017) The role of phytosphingosine-1-phosphate (Phyto-S1P) and its relationships with cytosolic pH and hydrogen peroxide (H2O2) during stomatal closure by darkness in broad bean. South African Journal of Botany 108, 237–242.
The role of phytosphingosine-1-phosphate (Phyto-S1P) and its relationships with cytosolic pH and hydrogen peroxide (H2O2) during stomatal closure by darkness in broad bean.Crossref | GoogleScholarGoogle Scholar |

Mishra G, Zhang WH, Deng F, Zhao J, Wang XM (2006) A bifurcating pathway directs abscisic acid effects on stomatal closure and opening in Arabidopsis. Science 312, 264–266.
A bifurcating pathway directs abscisic acid effects on stomatal closure and opening in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 16614222PubMed |

Molisch H (1937) Der Einfluss einer Pflanze auf die andere, Allelopathie. Fischer Jena.

Munemasa S, Oda K, Megumi WS, Nakamura Y, Shimoishi Y, Murata Y (2007) The coronatine-insensitive 1 mutation reveals the hormonal signaling interaction between abscisic acid and methyl jasmonate in Arabidopsis guard cells. Specific impairment of ion channel activation and second messenger production. Plant Physiology 143, 1398–1407.
The coronatine-insensitive 1 mutation reveals the hormonal signaling interaction between abscisic acid and methyl jasmonate in Arabidopsis guard cells. Specific impairment of ion channel activation and second messenger production.Crossref | GoogleScholarGoogle Scholar | 17220365PubMed |

Murata Y, Pei ZM, Mori IC, Schroeder J (2001) Abscisic acid activation of plasma membrane Ca2+ channels in guard cells requires cytosolic NAD(P)H and is differentially disrupted upstream and downstream of reactive oxygen species production in abi1–1 and abi2–1 protein phosphatase 2C mutants. The Plant Cell 13, 2513–2523.
Abscisic acid activation of plasma membrane Ca2+ channels in guard cells requires cytosolic NAD(P)H and is differentially disrupted upstream and downstream of reactive oxygen species production in abi1–1 and abi2–1 protein phosphatase 2C mutants.Crossref | GoogleScholarGoogle Scholar | 11701885PubMed |

Nagpal A, Hassan A, Ndamukong I, Avramova Z, Baluška F (2018) Myotubularins, PtdIns5P, and ROS in ABA-mediated stomatal movements in dehydrated Arabidopsis seedlings. Functional Plant Biology 45, 259–266.
Myotubularins, PtdIns5P, and ROS in ABA-mediated stomatal movements in dehydrated Arabidopsis seedlings.Crossref | GoogleScholarGoogle Scholar | 32291040PubMed |

Ohnishi N, Zhang LG, Sakamoto W (2018) VIPP1 involved in chloroplast membrane integrity has GTPase activity in vitro. Plant Physiology 177, 328–338.
VIPP1 involved in chloroplast membrane integrity has GTPase activity in vitro.Crossref | GoogleScholarGoogle Scholar | 29622686PubMed |

Pandey S (2017) Heterotrimeric G-protein regulatory circuits in plants: Conserved and novel mechanisms. Plant Signaling & Behavior
Heterotrimeric G-protein regulatory circuits in plants: Conserved and novel mechanisms.Crossref | GoogleScholarGoogle Scholar |

Qiao YJ, Gu CZ, Zhu HT, Wang D, Zhang MY, Zhang YX, Yang CR, Zhang YJ (2020) Allelochemicals of Panax notoginseng and their effects on various plants and rhizosphere microorganisms. Plant Diversity 42, 323–333.
Allelochemicals of Panax notoginseng and their effects on various plants and rhizosphere microorganisms.Crossref | GoogleScholarGoogle Scholar | 33134615PubMed |

Ren K, Hayat S, Qi X, Liu T, Cheng Z (2018) The garlic allelochemical DADS influences cucumber root growth involved in regulating hormone levels and modulating cell cycling. Journal of Plant Physiology 230, 51–60.
The garlic allelochemical DADS influences cucumber root growth involved in regulating hormone levels and modulating cell cycling.Crossref | GoogleScholarGoogle Scholar | 30170241PubMed |

Rice EL (2012) Allelopathy [M]. Academic press.

Sang Y, Zheng S, Li W, Huang B, Wang X (2001) Regulation of plant water loss by manipulating the expression of phospholipase Dα. The Plant Journal 28, 135–144.
Regulation of plant water loss by manipulating the expression of phospholipase Dα.Crossref | GoogleScholarGoogle Scholar | 11722757PubMed |

Schulz M, Kussmann P, Knop M, et al. (2007) Allelopathic monoterpenes interfere with Arabidopsis thaliana cuticular waxes and enhance transpiration. Plant Signaling & Behavior 2, 231–239.
Allelopathic monoterpenes interfere with Arabidopsis thaliana cuticular waxes and enhance transpiration.Crossref | GoogleScholarGoogle Scholar |

Singh D (2019) Allelochemical stress, ROS and plant defence system. International Journal of Biological Innovations. 1, 33–35.
Allelochemical stress, ROS and plant defence system.Crossref | GoogleScholarGoogle Scholar |

Sun L, Li YP, Miao WW, Piao TT, Hao Y, Hao FS (2017) NADK2 positively modulates abscisic acid-induced stomatal closure by affecting accumulation of H2O2, Ca2+ and nitric oxide in Arabidopsis guard cells. Plant Science 262, 81–90.
NADK2 positively modulates abscisic acid-induced stomatal closure by affecting accumulation of H2O2, Ca2+ and nitric oxide in Arabidopsis guard cells.Crossref | GoogleScholarGoogle Scholar | 28716423PubMed |

Tuteja N (2009) Signaling through G protein coupled receptors. Plant Signaling & Behavior 4, 942–947.
Signaling through G protein coupled receptors.Crossref | GoogleScholarGoogle Scholar |

Ullah N, Haq IU, Safdar N, Mirza B (2015) Physiological and biochemical mechanisms of allelopathy mediated by the allelochemical extracts of Phytolacca latbenia (Moq.) H. Walter. Toxicology and Industrial Health 31, 931–937.
Physiological and biochemical mechanisms of allelopathy mediated by the allelochemical extracts of Phytolacca latbenia (Moq.) H. Walter.Crossref | GoogleScholarGoogle Scholar | 23572390PubMed |

Uraji M, Katagiri T, Okuma E, Ye W, Hossain MA, Masuda C, Miura A, Nakamura Y, Mori IC, Shinozaki K (2012) Cooperative function of PLDδ and PLDα1 in abscisic acid-induced stomatal closure in Arabidopsis. Plant Physiology 159, 450–460.
Cooperative function of PLDδ and PLDα1 in abscisic acid-induced stomatal closure in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 22392280PubMed |

Wang H, Liang X, Huang J, Zhang D, Lu H, Liu Z, Bi Y (2010) Involvement of ethylene and hydrogen peroxide in induction of alternative respiratory pathway in salt-treated Arabidopsis calluses. Plant & Cell Physiology 51, 1754–1765.
Involvement of ethylene and hydrogen peroxide in induction of alternative respiratory pathway in salt-treated Arabidopsis calluses.Crossref | GoogleScholarGoogle Scholar |

Wang L, Wan R, Shi Y, Xue S (2016) Hydrogen sulfide activates s-Type anion channel via OST1 and Ca2+ Modules. Molecular Plant
Hydrogen sulfide activates s-Type anion channel via OST1 and Ca2+ Modules.Crossref | GoogleScholarGoogle Scholar | 28007557PubMed |

Wang W, Wang X, Huang M, Cai J, Zhou Q, Dai T, Cao W, Jiang D (2018) Hydrogen peroxide and abscisic acid mediate salicylic acid-induced freezing tolerance in wheat. Frontiers in Plant Science 9, 1137
Hydrogen peroxide and abscisic acid mediate salicylic acid-induced freezing tolerance in wheat.Crossref | GoogleScholarGoogle Scholar | 30123235PubMed |

Yan S, Luo ST, Dong SS, Zhang T, Sun JG, Wang NG, Yao HJ, Shen YB (2015) Heterotrimeric G-proteins involved in the MeJA regulated ion flux and stomatal closure in Arabidopsis thaliana. Functional Plant Biology 42, 126–135.
Heterotrimeric G-proteins involved in the MeJA regulated ion flux and stomatal closure in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 32480659PubMed |

Yan Y, Zhang WN, Li YS, He CX, Gao LH, Yu XC (2018) Functions of CsGPA1 on the hypocotyl elongation and root growth of cucumbers. Scientific Reports 8, 15583
Functions of CsGPA1 on the hypocotyl elongation and root growth of cucumbers.Crossref | GoogleScholarGoogle Scholar | 30349017PubMed |

Yan Y, Sun MT, Li YS, Wang J, He CX, Yu XC (2020) The CsGPA1-CsAQPs module is essential for salt tolerance of cucumber seedlings. Plant Cell Reports 39, 1301–1316.
The CsGPA1-CsAQPs module is essential for salt tolerance of cucumber seedlings.Crossref | GoogleScholarGoogle Scholar | 32648011PubMed |

Yang N, Ding FX, Wu GF, Wang CL, Ding L, An LZ (2015) Phospholipase Dα from Chorispora bungeana: cloning and partial functional characterization. Plant Growth Regulation 75, 511–520.
Phospholipase Dα from Chorispora bungeana: cloning and partial functional characterization.Crossref | GoogleScholarGoogle Scholar |

Yuliyani ED, Darmanti S, Hastuti ED (2019) Allelochemical effects of Chromolaena odorata L. against photosynthetic pigments and stomata of Ageratum conyzoides L. leaves. Journal of Physics: Conference Series 1217, 012149
Allelochemical effects of Chromolaena odorata L. against photosynthetic pigments and stomata of Ageratum conyzoides L. leaves.Crossref | GoogleScholarGoogle Scholar |

Zhang L, Hu G, Cheng Y, Huang J (2008) Heterotrimeric G protein alpha and beta subunits antagonistically modulate stomatal density in Arabidopsis thaliana. Developmental Biology 324, 68–75.
Heterotrimeric G protein alpha and beta subunits antagonistically modulate stomatal density in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 18834874PubMed |

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 | 19690149PubMed |

Zhou BL, Chen F, Liu N, Wu Q, Lu Bo (2010) Allelopathy of diisobutyl phthalate to Verticillium wilt and seedling growth of eggplant. Xibei Nongye Xuebao 4, 179–183.
Allelopathy of diisobutyl phthalate to Verticillium wilt and seedling growth of eggplant.Crossref | GoogleScholarGoogle Scholar |