Ca2+ signal contributing to jasmonic acid‐induced direct and indirect defense against the whitefly Bemisia tabaci in tomato plants

The phytophagous whitefly Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) causes serious crop yield losses around the world especially by vectoring viruses. Exogenous jasmonic acid (JA) induces direct plant resistance to B. tabaci, but the underlying mechanism of JA‐induced exogenous defenses is not well understood. Here, we demonstrate that exogenous JA not only increases the cytosolic Ca2+ concentration ([Ca2+]cyt) in tomato mesophyll cells but also induces the expression of Ca2+‐sensor genes and plant defense genes. Pre‐treatment with Ca2+ inhibitor (ruthenium red) significantly repressed the elevation of [Ca2+]cyt, expression of JA‐induced genes, and emission of plant volatiles induced by JA, thus reducing the JA‐induced direct (feeding choice and fitness of B. tabaci) and indirect [olfactory choice and parasitism by the parasitoid Encarsia formosa Gahan (Hymenoptera: Aphelinidae)] plant resistance to B. tabaci. These results indicate that the Ca2+ signal induced by JA mediates and directs the plants defenses against whitefly. Present results will not only give us a better understanding of how exogenous JA influences the crop community, but also deliver some clues for the potential application of exogenous JA, as a plant elicitor, in whitefly management.

[1]  S. Luan,et al.  Calcium spikes, waves and oscillations in plant development and biotic interactions , 2020, Nature Plants.

[2]  S. Luan,et al.  The CBL-CIPK Calcium Signaling Network: Unified Paradigm from 20 Years of Discoveries. , 2020, Trends in plant science.

[3]  M. Erb,et al.  Induction of defense in cereals by 4-fluorophenoxyacetic acid suppresses insect pest populations and increases crop yields in the field , 2020, Proceedings of the National Academy of Sciences.

[4]  Youjun Zhang,et al.  Direct and indirect plant defenses induced by (Z)-3-hexenol in tomato against whitefly attack , 2020, Journal of Pest Science.

[5]  Shaoli Wang,et al.  Comparative transcriptome analysis of differentially expressed genes in Bradysia odoriphaga Yang et Zhang (Diptera: Sciaridae) at different acute stress temperatures. , 2020, Genomics.

[6]  Shaoli Wang,et al.  A salivary ferritin in the whitefly suppresses plant defenses and facilitates host exploitation , 2019, Journal of experimental botany.

[7]  M. Dicke,et al.  Airborne host–plant manipulation by whiteflies via an inducible blend of plant volatiles , 2019, Proceedings of the National Academy of Sciences.

[8]  M. Erb,et al.  Molecular Dissection of Early Defense Signaling Underlying Volatile-Mediated Defense Regulation and Herbivore Resistance in Rice[OPEN] , 2019, Plant Cell.

[9]  Yanwei Sun,et al.  A whitefly effector Bsp9 targets host immunity regulator WRKY33 to promote performance , 2019, Philosophical Transactions of the Royal Society B.

[10]  Xiaowei Wang,et al.  A salivary effector enables whitefly to feed on host plants by eliciting salicylic acid-signaling pathway , 2018, Proceedings of the National Academy of Sciences.

[11]  Pengjun Zhang,et al.  Jasmonic Acid-Dependent Defenses Play a Key Role in Defending Tomato Against Bemisia tabaci Nymphs, but Not Adults , 2018, Front. Plant Sci..

[12]  D. Xie,et al.  Injury Activates Ca2+/Calmodulin-Dependent Phosphorylation of JAV1-JAZ8-WRKY51 Complex for Jasmonate Biosynthesis. , 2018, Molecular cell.

[13]  C. Foyer,et al.  A Plant Phytosulfokine Peptide Initiates Auxin-Dependent Immunity through Cytosolic Ca2+ Signaling in Tomato[OPEN] , 2018, Plant Cell.

[14]  C. Mazars,et al.  Calcium Signalling in Plant Biotic Interactions , 2018, International journal of molecular sciences.

[15]  Shaoli Wang,et al.  Different effects of exogenous jasmonic acid on preference and performance of viruliferous Bemisia tabaci B and Q , 2017 .

[16]  Shaoli Wang,et al.  Virus-Infected Plants Altered the Host Selection of Encarsia formosa, a Parasitoid of Whiteflies , 2017, Front. Physiol..

[17]  Shaoli Wang,et al.  Odor, Not Performance, Dictates Bemisia tabaci's Selection between Healthy and Virus Infected Plants , 2017, Front. Physiol..

[18]  M. Mescher,et al.  Tomato yellow leaf curl virus differentially influences plant defence responses to a vector and a non-vector herbivore. , 2016, Plant, cell & environment.

[19]  M. Dicke,et al.  Volatile-mediated foraging behaviour of three parasitoid species under conditions of dual insect herbivore attack , 2016, Animal Behaviour.

[20]  M. Maffei,et al.  Role of early signalling events in plant-insect interactions. , 2015, Journal of experimental botany.

[21]  T. Eulgem,et al.  Synthetic plant defense elicitors , 2015, Front. Plant Sci..

[22]  Y. Jing,et al.  Effect of Ca2+ on Mediating the MeJA-induced Synthesis of Triterpenoid in Suspension Cells of Betula platyphylla Suk. , 2015 .

[23]  D. Gerling,et al.  Whitefly parasitoids: distribution, life history, bionomics, and utilization. , 2015, Annual review of entomology.

[24]  M. Erb,et al.  The prospect of applying chemical elicitors and plant strengtheners to enhance the biological control of crop pests , 2014, Philosophical Transactions of the Royal Society B: Biological Sciences.

[25]  Shaoli Wang,et al.  Plant Virus Differentially Alters the Plant's Defense Response to Its Closely Related Vectors , 2013, PloS one.

[26]  Baoli Qiu,et al.  Root and shoot jasmonic acid induced plants differently affect the performance of Bemisia tabaci and its parasitoid Encarsia formosa , 2013 .

[27]  Pengjun Zhang,et al.  Feeding by Whiteflies Suppresses Downstream Jasmonic Acid Signaling by Eliciting Salicylic Acid Signaling , 2013, Journal of Chemical Ecology.

[28]  Shaoli Wang,et al.  Multiple Forms of Vector Manipulation by a Plant-Infecting Virus: Bemisia tabaci and Tomato Yellow Leaf Curl Virus , 2013, Journal of Virology.

[29]  P. J. Barro,et al.  Species Concepts as Applied to the Whitefly Bemisia tabaci Systematics: How Many Species Are There? , 2012 .

[30]  Youjun Zhang Further spread of and domination by Bemisia tabaci biotype Q on field crops in China , 2011 .

[31]  You Zhang,et al.  Cryptic Invasion of the Exotic Bemisia tabaci Biotype Q Occurred Widespread in Shandong Province of China , 2010 .

[32]  G. Devine,et al.  Insecticide resistance in Bemisia tabaci biotype Q (Hemiptera: Aleyrodidae) from China , 2010 .

[33]  Qingpeng Sun,et al.  Extracellular and Intracellular Calcium both Involved in the Jasmonic Acid Induced Calcium Mobilization in Arabidopsis thaliana , 2010 .

[34]  L. Walling,et al.  Silverleaf Whitefly Induces Salicylic Acid Defenses and Suppresses Effectual Jasmonic Acid Defenses1[W][OA] , 2006, Plant Physiology.

[35]  B. Cong,et al.  THE INTRODUCTION OF THE EXOTIC Q BIOTYPE OF BEMISIA TABACI FROM THE MEDITERRANEAN REGION INTO CHINA ON ORNAMENTAL CROPS , 2006 .

[36]  Daye Sun,et al.  Influx of extracellular Ca2+ involved in jasmonic-acid-induced elevation of [Ca2+]cyt and JR1 expression in Arabidopsis thaliana , 2006, Journal of Plant Research.

[37]  David R. Jones Plant Viruses Transmitted by Whiteflies , 2003, European Journal of Plant Pathology.

[38]  D. Gerling,et al.  Biological control of Bemisia tabaci using predators and parasitoids , 2001 .

[39]  E. Johannes,et al.  Systemin triggers an increase of cytoplasmic calcium in tomato mesophyll cells: Ca2+ mobilization from intra‐ and extracellular compartments , 1998 .

[40]  A. Trewavas,et al.  Cold calcium signaling in Arabidopsis involves two cellular pools and a change in calcium signature after acclimation. , 1996, The Plant cell.

[41]  L. Boykin,et al.  Bemisia tabaci: a statement of species status. , 2011, Annual review of entomology.

[42]  Fu-kuan Zhao,et al.  Is there crosstalk between extracellular and intracellular calcium mobilization in jasmonic acid signaling , 2008, Plant Growth Regulation.

[43]  Luo Chen The use of mitochondrial cytochrome oxidase I(mt COI)gene sequences for the identification of biotypes of Bemisia tabaci(Gennadius)in China , 2002 .

[44]  H. Czosnek,et al.  Whitefly transmission of plant viruses , 2002 .