Chin Bull Bot ›› 2019, Vol. 54 ›› Issue (2): 255-264.doi: 10.11983/CBB18152


• SPECIAL TOPICS • Previous Articles     Next Articles

Plant Systemic Signaling Under Biotic and Abiotic Stresses Conditions

Dai Yujia1,2,Luo Xiaofeng1,2,Zhou Wenguan1,2,Chen Feng1,2,Shuai Haiwei1,Yang Wenyu1,*(),Shu Kai1,2,*()   

  1. 1 Key Laboratory of Crop Ecophysiology and Farming System in Southwest China, Ministry of Agriculture, Institute of Ecological Agriculture, College of Agronomy, Sichuan Agricultural University, Chengdu 611130, China
    2 Center for Ecological and Environmental Sciences, Northwestern Polytechnical University, Xi’an 710129, China
  • Received:2018-07-08 Accepted:2018-12-10 Online:2019-09-01 Published:2019-03-01
  • Contact: Yang Wenyu,Shu Kai;


Plants have evolved numerous strategies to adapt to complex and changing surroundings. Plants have a wide range of systemic responses induced by local stresses to precisely regulate plant growth, development and adaptability to environments. Plant systemic responses induce whole-plant signaling transmission at first, called systemic signaling. When subjected to local stresses, plants trigger chemical molecules in local cells, such as biosynthesis and/or signaling transduction of the phytohormones jasmonic acid and methyl salicylate. Accompanied by a series of complex signal cascades, multiple signal components work together to activate the systemic response. In the past several years, pioneer studies demonstrated that phytohormones, small peptides and several types of RNAs are considered key components of slow-moving systemic signaling, and rapid systemic signals include reactive oxygen species, calcium signals and electrical signals. Plant systemic signaling is essential for plant growth, development and adaptation to the environment, and the precise transmission mechanism is worthy of further investigation. In this review, we describe the research progress in plant systemic signaling transmission and response to the environment and summarize several key systemic signal components and their transmission mechanism. Finally, the potential challenges of future research in this research field are discussed.

Key words: systemic signaling, jasmonic acid, salicylic acid, RNA, reactive oxygen species

Table 1

Important components of plant systemic signaling"

信号组分 作用方式 参考文献
激素类 茉莉酸(JA) 响应创伤、寒冷和昆虫啃食等, 在植物体内发生系
Koo et al., 2009; VanDoorn et al., 2011; Yan et al., 2013
响应病原菌侵染, 调控植物免疫反应 Mou et al., 2003; Lee et al., 2015; Ali et al., 2017
油菜素甾醇(BR) 与系统信号组件互作, 调控系统响应, 如活性氧 Xia et al., 2011, 2015
RNA 响应多种胁迫, 作为基因表达产物在维管束中系
Yoo et al., 2004; Suzuki et al., 2015
小分子肽 系统素 广泛存在于茄科植物中, 提高植株对植食性动物
Scheer et al., 2003; Coppola et al., 2017
环二肽 增强植物对病原菌和病毒侵害的抵抗力, 诱导活
Wu et al., 2017
在维管束中, 如壬二酸和哌啶酸, 引起SA的积累,
Jung et al., 2009; Shah et al., 2014
MeSA 在维管束中, SA的代谢产物, 是重要的系统信号分子 Park et al., 2007
活性氧 迅速产生并响应多种胁迫, 是从胞间信号到系统信
Dat et al., 2000; Hancock et al., 2001; Czarnocka and Karpinski, 2018
Ca2+ 迅速产生并响应多种胁迫, 细胞内重要的第二信
使, 具有信号转导迅速和分布广泛的特征
Ranty et al., 2016; Zhu, 2016
电信号 响应创伤和昆虫啃咬等, 以高效的信息传递功能与
Vincill et al., 2012; Gilroy et al., 2016; Hedrich et al., 2016; Szechyńska- Hebda et al., 2017
其它 离子通道 如GLR和TPC, 调控电信号和Ca2+等快速信号的胞
间传递, 也为多种信号的偶联提供可能
Miller et al., 2009; Choi et al., 2016; Gilroy et al., 2016
RBOH 是调控活性氧信号转导的关键酶类 Miller et al., 2009; Mittler, 2017
NPR1 SA受体, 是SA信号通路的关键组分 Mou et al., 2003; Niu et al., 2016; Ali et al., 2017
[1] 帅海威, 孟永杰, 陈锋, 周文冠, 罗晓峰, 杨文钰, 舒凯 ( 2018). 植物荫蔽胁迫的激素信号响应. 植物学报 53, 139-148.
[2] Ali S, Mir ZA, Tyagi A, Mehari H, Meena RP, Bhat JA, Yadav P, Papalou P, Rawat S, Grover A ( 2017). Over- expression of NPR1 in Brassica juncea confers broad spectrum resistance to fungal pathogens. Front Plant Sci 8, 1693.
[3] Allu AD, Brotman Y, Xue GP, Balazadeh S ( 2016). Trans- cription factor ANAC032 modulates JA/SA signaling in response to Pseudomonas syringae infection. EMBO Rep 17, 1578-1589.
[4] Ananieva EA, Christov KN, Popova LP ( 2004). Exogenous treatment with salicylic acid leads to increased antioxidant capacity in leaves of barley plants exposed to paraquat. J Plant Physiol 161, 319-328.
doi: 10.1078/0176-1617-01022
[5] Betsuyaku S, Katou S, Takebayashi Y, Sakakibara H, Nomura N, Fukuda H ( 2018). Salicylic acid and jasmonic acid pathways are activated in spatially different domains around the infection site during effector-triggered immunity in Arabidopsis thaliana . Plant Cell Physiol 59, 8-16.
[6] Bourtsala A, Dafnis I, Chroni A, Farmaki T, Galanopoulou D ( 2018). Study of the involvement of phosphatidic acid formation in the expression of wound-responsive genes in cotton. Lipids 53, 589-599.
doi: 10.1002/lipd.2018.53.issue-6
[7] Caarls L, Pieterse CMJ, Van Wees SCM ( 2015). How salicylic acid takes transcriptional control over jasmonic acid signaling. Front Plant Sci 6, 170.
[8] Casal JJ ( 2012). Shade avoidance. Arabidopsis Book 10, e0157.
doi: 10.1199/tab.0157
[9] Chen ZX, Zheng ZY, Huang JL, Lai ZB, Fan BF ( 2009). Biosynthesis of salicylic acid in plants. Plant Signal Behav 4, 493-496.
doi: 10.4161/psb.4.6.8392
[10] Chiou TJ, Lin SI ( 2011). Signaling network in sensing phosphate availability in plants. Annu Rev Plant Biol 62, 185-206.
doi: 10.1146/annurev-arplant-042110-103849
[11] Choi WG, Hilleary R, Swanson SJ, Kim SH, Gilroy S ( 2016). Rapid, long-distance electrical and calcium signa- ling in plants. Annu Rev Plant Biol 67, 287-307.
doi: 10.1146/annurev-arplant-043015-112130
[12] Choi WG, Miller G, Wallace I, Harper J, Mittler R, Gilroy S ( 2017). Orchestrating rapid long-distance signaling in plants with Ca 2+, ROS and electrical signals . Plant J 90, 698-707.
doi: 10.1111/tpj.2017.90.issue-4
[13] Choi WG, Toyota M, Kim SH, Hilleary R, Gilroy S ( 2014). Salt stress-induced Ca 2+ waves are associated with rapid, long-distance root-to-shoot signaling in plants . Proc Natl Acad Sci USA 111, 6497-6502.
doi: 10.1073/pnas.1319955111
[14] Coppola M, Cascone P, Madonna V, Di Lelio I, Esposito F, Avitabile C, Romanelli A, Guerrieri E, Vitiello A, Pen- nacchio F, Rao R, Corrado G ( 2017). Plant-to-plant communication triggered by systemin primes antiher- bivore resistance in tomato. Sci Rep 7, 15522.
doi: 10.1038/s41598-017-15481-8
[15] Czarnocka W, Karpinski S ( 2018). Friend or foe? Reactive oxygen species production, scavenging and signaling in plant response to environmental stresses. Free Radic Biol Med 122, 4-20.
doi: 10.1016/j.freeradbiomed.2018.01.011
[16] Dat J, Vandenabeele S, Vranová E, Van Montagu M, Inzé D, Van Breusegem F ( 2000). Dual action of the active oxygen species during plant stress responses. Cell Mol Life Sci 57, 779-795.
doi: 10.1007/s000180050041
[17] Ding CK, Wang C, Gross KC, Smith DL ( 2002). Jasmonate and salicylate induce the expression of pathogenesis- related-protein genes and increase resistance to chilling injury in tomato fruit. Planta 214, 895-901.
doi: 10.1007/s00425-001-0698-9
[18] Durrant WE, Dong X ( 2004). Systemic acquired resistance. Annu Rev Phytopathol 42, 185-209.
doi: 10.1146/annurev.phyto.42.040803.140421
[19] Fu ZQ, Dong XN ( 2013). Systemic acquired resistance: turning local infection into global defense. Annu Rev Plant Biol 64, 839-863.
doi: 10.1146/annurev-arplant-042811-105606
[20] Gaupels F, Durner J, Kogel KH ( 2017). Production, ampli- fication and systemic propagation of redox messengers in plants? The phloem can do it all! New Phytol 214, 554-560.
doi: 10.1111/nph.14399
[21] Gechev TS, Van Breusegem F, Stone JM, Denev I, Laloi C ( 2006). Reactive oxygen species as signals that modulate plant stress responses and programmed cell death. Bioes- says 28, 1091-1101.
doi: 10.1002/(ISSN)1521-1878
[22] Gilroy S, Bialasek M, Suzuki N, Górecka M, Devireddy AR, Karpiński S, Mittler R ( 2016). ROS, calcium, and electric signals: key mediators of rapid systemic signaling in plants. Plant Physiol 171, 1606-1615.
doi: 10.1104/pp.16.00434
[23] Gilroy S, Suzuki N, Miller G, Choi WG, Toyota M, Devi- reddy AR, Mittler R ( 2014). A tidal wave of signals: calcium and ROS at the forefront of rapid systemic sig- naling. Trends Plant Sci 19, 623-630.
doi: 10.1016/j.tplants.2014.06.013
[24] Gorecka M, Alvarez-Fernandez R, Slattery K, McAusland L, Davey PA, Karpinski S, Lawson T, Mullineaux PM ( 2014). Abscisic acid signaling determines susceptibility of bundle sheath cells to photoinhibition in high light-exposed Arabidopsis leaves. Philos Trans R Soc Lond B Biol Sci 369, 20130234.
doi: 10.1098/rstb.2013.0234
[25] Ham BK, Lucas WJ ( 2017). Phloem-mobile RNAs as sys- temic signaling agents. Annu Rev Plant Biol 68, 173-195.
doi: 10.1146/annurev-arplant-042916-041139
[26] Han HN, Wang Q, Wei L, Liang Y, Dai JL, Xia GM, Liu SW ( 2018). Small RNA and degradome sequencing used to elucidate the basis of tolerance to salinity and alkalinity in wheat. BMC Plant Biol 18, 195.
doi: 10.1186/s12870-018-1415-1
[27] Hancock JT, Desikan R, Neill SJ ( 2001). Role of reactive oxygen species in cell signaling pathways. Biochem Soc Trans 29, 345-349.
doi: 10.1042/bst0290345
[28] He X, Jiang JS, Wang CQ, Dehesh K ( 2017). ORA59 and EIN3 interaction couples jasmonate-ethylene synergistic action to antagonistic salicylic acid regulation of PDF exp- ression. J Integr Plant Biol 59, 275-287.
doi: 10.1111/jipb.12524
[29] Hedrich R, Salvador-Recatalà V, Dreyer I ( 2016). Electrical wiring and long-distance plant communication. Trends Plant Sci 21, 376-387.
doi: 10.1016/j.tplants.2016.01.016
[30] Hepler PK ( 2005). Calcium: a central regulator of plant growth and development. Plant Cell 17, 2142-2155.
doi: 10.1105/tpc.105.032508
[31] Hilleary R, Gilroy S ( 2018). Systemic signaling in response to wounding and pathogens. Curr Opin Plant Biol 43, 57-62.
doi: 10.1016/j.pbi.2017.12.009
[32] Jung HW, Tschaplinski TJ, Wang L, Glazebrook J, Green- berg JT ( 2009). Priming in systemic plant immunity. Science 324, 89-91.
doi: 10.1126/science.1170025
[33] Kadota Y, Shirasu K, Zipfel C ( 2015). Regulation of the NADPH oxidase RBOHD during plant immunity. Plant Cell Physiol 56, 1472-1480.
doi: 10.1093/pcp/pcv063
[34] Karpinski S, Reynolds H, Karpinska B, Wingsle G, Creissen G, Mullineaux P ( 1999). Systemic signaling and acclimation in response to excess excitation energy in Arabidopsis. Science 284, 654-657.
doi: 10.1126/science.284.5414.654
[35] Konert G, Rahikainen M, Trotta A, Kangasjärvi S ( 2013). Systemic signaling in light acclimation of leaves. In: Baluška F, ed. Long-distance Systemic Signaling and Communication in Plants. Signaling and Communication in Plants, Vol. 19. Berlin, Heidelberg: Springer. pp. 231-250.
doi: 10.1007/978-3-642-36470-9
[36] Koo AJK, Gao XL, Jones AD, Howe GA ( 2009). A rapid wound signal activates the systemic synthesis of bioactive jasmonates in Arabidopsis. Plant J 59, 974-986.
doi: 10.1111/tpj.2009.59.issue-6
[37] Koo AJK, Howe GA ( 2009). The wound hormone jasmonate. Phytochemistry 70, 1571-1580.
doi: 10.1016/j.phytochem.2009.07.018
[38] Kooijman EE, Burger KNJ ( 2009). Biophysics and function of phosphatidic acid: a molecular perspective. Biochim Biophys Acta 1791, 881-888.
doi: 10.1016/j.bbalip.2009.04.001
[39] Kosová K, Vitámvás P, Prášil IT, Renaut J ( 2011). Plant proteome changes under abiotic stress—contribution of proteomics studies to understanding plant stress res- ponse. J Proteomics 74, 1301-1322.
doi: 10.1016/j.jprot.2011.02.006
[40] Kudla J, Becker D, Grill E, Hedrich R, Hippler M, Kummer U, Parniske M, Romeis T, Schumacher K ( 2018). Advan- ces and current challenges in calcium signaling. New Phytol 218, 414-431.
doi: 10.1111/nph.14966
[41] LeBrasseur ND, MacIntosh GC, Pérez-Amador MA, Sai- toh M, Green PJ ( 2002). Local and systemic wound- induction of RNase and nuclease activities in Arabidopsis: RNS1 as a marker for a JA-independent systemic sig- naling pathway. Plant J 29, 393-403.
doi: 10.1046/j.1365-313x.2002.01223.x
[42] Lee HJ, Park YJ, Seo PJ, Kim JH, Sim HJ, Kim SG, Park CM ( 2015). Systemic immunity requires SnRK2.8-media- ted nuclear import of NPR1 in Arabidopsis. Plant Cell 27, 3425-3438.
doi: 10.1105/tpc.15.00371
[43] Li YZ, Qin L, Zhao JJ, Muhammad T, Cao HH, Li HL, Zhang Y, Liang Y ( 2017). SlMAPK3 enhances tolerance to tomato yellow leaf curl virus (TYLCV) by regulating salicylic acid and jasmonic acid signaling in tomato( Sol- anum lycopersicum). PLoS One 12, e0172466.
[44] Lucas WJ, Groover A, Lichtenberger R, Furuta K, Yadav SR, Helariutta Y, He XQ, Fukuda H, Kang J, Brady SM, Patrick JW, Sperry J, Yoshida A, López-Millán AF, Grusak MA, Kachroo P ( 2013). The plant vascular sys- tem: evolution, development and functions. J Integr Plant Biol 55, 294-388.
doi: 10.1111/jipb.2013.55.issue-4
[45] Machado RAR, Robert CAM, Arce CCM, Ferrieri AP, Xu SQ, Jimenez-Aleman GH, Baldwin IT, Erb M ( 2016). Auxin is rapidly induced by herbivore attack and regulates a subset of systemic, jasmonate-dependent defenses. Plant Physiol 172, 521-532.
doi: 10.1104/pp.16.00940
[46] McConn M, Creelman RA, Bell E, Mullet JE, Browse J ( 1997). Jasmonate is essential for insect defense in Ara- bidopsis. Proc Natl Acad Sci USA 94, 5473-5477.
doi: 10.1073/pnas.94.10.5473
[47] Miller G, Schlauch K, Tam R, Cortes D, Torres MA, Shu- laev V, Dangl JL, Mittler R ( 2009). The plant NADPH oxidase RBOHD mediates rapid systemic signaling in response to diverse stimuli. Sci Signal 2, ra45.
[48] Mittler R ( 2017). ROS are good. Trends Plant Sci 22, 11-19.
doi: 10.1016/j.tplants.2016.08.002
[49] Mittler R, Vanderauwera S, Suzuki N, Miller G, Tognetti VB, Vandepoele K, Gollery M, Shulaev V, Van Breuse- gem F ( 2011). ROS signaling: the new wave? Trends Plant Sci 16, 300-309.
doi: 10.1016/j.tplants.2011.03.007
[50] Mou ZL, Fan WH, Dong XN ( 2003). Inducers of plant sys- temic acquired resistance regulate NPR1 function through redox changes. Cell 113, 935-944.
doi: 10.1016/S0092-8674(03)00429-X
[51] Mousavi SAR, Chauvin A, Pascaud F, Kellenberger S, Farmer EE ( 2013). GLUTAMATE RECEPTOR-LIKE ge- nes mediate leaf-to-leaf wound signaling. Nature 500, 422-426.
[52] Niu DD, Wang XJ, Wang YR, Song XO, Wang JS, Guo JH, Zhao HW ( 2016). Bacillus cereus AR156 activates PAMP- triggered immunity and induces a systemic acquired resistance through a NPR1- and SA-dependent signaling pathway. Biochem Biophys Res Commun 469, 120-125.
[53] Notaguchi M, Okamoto S ( 2015). Dynamics of long-distance signaling via plant vascular tissues. Front Plant Sci 6, 161.
[54] Park SW, Kaimoyo E, Kumar D, Mosher S, Klessig DF ( 2007). Methyl salicylate is a critical mobile signal for plant systemic acquired resistance. Science 318, 113-116.
doi: 10.1126/science.1147113
[55] Ramachandran P, Wang GD, Augstein F, De Vries J, Carlsbecker A ( 2018). Continuous root xylem formation and vascular acclimation to water deficit involves endoder- mal ABA signaling via miR165. Development 145, dev 159202.
[56] Ranty B, Aldon D, Cotelle V, Galaud JP, Thuleau P, Maz- ars C ( 2016). Calcium sensors as key hubs in plant respon- ses to biotic and abiotic stresses. Front Plant Sci 7, 327.
[57] Rasmann S, De Vos M, Casteel CL, Tian DL, Halitschke R, Sun JY, Agrawal AA, Felton GW, Jander G ( 2012). Her- bivory in the previous generation primes plants for en- hanced insect resistance. Plant Physiol 158, 854-863.
doi: 10.1104/pp.111.187831
[58] Scheer JM, Pearce G, Ryan CA ( 2003). Generation of systemin signaling in tobacco by transformation with the tomato systemin receptor kinase gene. Proc Natl Acad Sci USA 100, 10114-10117.
doi: 10.1073/pnas.1432910100
[59] Shah J, Chaturvedi R, Chowdhury Z, Venables B, Petros RA ( 2014). Signaling by small metabolites in systemic acquired resistance. Plant J 79, 645-658.
doi: 10.1111/tpj.2014.79.issue-4
[60] Shu K, Qi Y, Chen F, Meng YJ, Luo XF, Shuai HW, Zhou WG, Ding J, Du JB, Liu J, Yang F, Wang Q, Liu WG, Yong TW, Wang XC, Feng YQ, Yang WY ( 2017). Salt stress represses soybean seed germination by negatively regulating GA biosynthesis while positively mediating ABA biosynthesis. Front Plant Sci 8, 1372.
doi: 10.3389/fpls.2017.01372
[61] Shu K, Zhou WG, Chen F, Luo XF, Yang WY ( 2018). Absci- sic acid and gibberellins antagonistically mediate plant development and abiotic stress responses. Front Plant Sci 9, 416.
doi: 10.3389/fpls.2018.00416
[62] Smirnova E, Marquis V, Poirier L, Aubert Y, Zumsteg J, Ménard R, Miesch L, Heitz T ( 2017). Jasmonic acid oxidase 2 hydroxylates jasmonic acid and represses basal defense and resistance responses against Botrytis cinerea infection. Mol Plant 10, 1159-1173.
[63] Song GC, Choi HK, Ryu CM ( 2015). Gaseous 3-pentanol primes plant immunity against a bacterial speck pathogen, Pseudomonas syringae pv. tomato via salicylic acid and jasmonic acid-dependent signaling pathways in Arabidop- sis. Front Plant Sci 6, 821.
[64] Stephens NR, Qi Z, Spalding EP ( 2008). Glutamate re- ceptor subtypes evidenced by differences in desensiti- zation and dependence on the GLR3.3 and GLR3.4 genes. Plant Physiol 146, 529-538.
[65] Suzuki N, Devireddy AR, Inupakutika MA, Baxter A, Miller G, Song L, Shulaev E, Azad RK, Shulaev V, Mittler R ( 2015). Ultra-fast alterations in mRNA levels uncover mul- tiple players in light stress acclimation in plants. Plant J 84, 760-772.
doi: 10.1111/tpj.13039
[66] Szczegielniak J, Borkiewicz L, Szurmak B, Lewand ows- ka-Gnatowska E, Statkiewicz M, Klimecka M, Cie?la J, Muszyńska G ( 2012). Maize calcium-dependent protein kinase (ZmCPK11): local and systemic response to woun- ding, regulation by touch and components of jasmonate signaling. Physiol Plant 146, 1-14.
doi: 10.1111/ppl.2012.146.issue-1
[67] Szechyńska-Hebda M, Lewandowska M, Karpiński S ( 2017). Electrical signaling, photosynthesis and systemic acquired acclimation. Front Physiol 8, 684.
doi: 10.3389/fphys.2017.00684
[68] Takahashi F, Suzuki T, Osakabe Y, Betsuyaku S, Kondo Y, Dohmae N, Fukuda H, Yamaguchi-Shinozaki K, Shinozaki K ( 2018). A small peptide modulates stomatal control via abscisic acid in long-distance signaling. Nature 556, 235-238.
doi: 10.1038/s41586-018-0009-2
[69] Tian YC, Fan M, Qin ZX, Lv HJ, Wang MM, Zhang Z, Zhou WY, Zhao N, Li XH, Han C, Ding ZJ, Wang WF, Wang ZY, Bai MY ( 2018). Hydrogen peroxide positively regula- tes brassinosteroid signaling through oxidation of the BRASSINAZOLE-RESISTANT1 transcription factor. Nat Commun 9, 1063.
doi: 10.1038/s41467-018-03463-x
[70] Tsutsui H, Notaguchi M ( 2017). The use of grafting to study systemic signaling in plants. Plant Cell Physiol 58, 1291-1301.
doi: 10.1093/pcp/pcx098
[71] Van Breusegem F, Bailey-Serres J, Mittler R ( 2008). Unra- veling the tapestry of networks involving reactive oxygen species in plants. Plant Physiol 147, 978-984.
doi: 10.1104/pp.108.122325
[72] Van Der Does D, Leon-Reyes A, Koornneef A, Van Verk MC, Rodenburg N, Pauwels L, Goossens A, Körbes AP, Memelink J, Ritsema T, Van Wees SCM, Pieterse CMJ ( 2013). Salicylic acid suppresses jasmonic acid signaling downstream of SCF COI1-JAZ by targeting GCC promoter motifs via transcription factor ORA59 . Plant Cell 25, 744-761.
doi: 10.1105/tpc.112.108548
[73] VanDoorn A, Bonaventure G, Schmidt DD, Baldwin IT ( 2011). Regulation of jasmonate metabolism and activa- tion of systemic signaling in Solanum nigrum : COI1 and JAR4 play overlapping yet distinct roles. New Phytol 190, 640-652.
[74] Vashegyi I, Marozsán-Tóth Z, Galiba G, Dobrev PI, Vankova R, Tóth B ( 2013). Cold response of dedifferen- tiated barley cells at the gene expression, hormone composition, and freezing tolerance levels: studies on callus cultures. Mol Biotechnol 54, 337-349.
doi: 10.1007/s12033-012-9569-9
[75] Vincill ED, Bieck AM, Spalding EP ( 2012). Ca 2+ conduction by an amino acid-gated ion channel related to glutamate receptors . Plant Physiol 159, 40-46.
doi: 10.1104/pp.112.197509
[76] Vlot AC, Klessig DF, Park SW ( 2008). Systemic acquired resistance: the elusive signal(s). Curr Opin Plant Biol 11, 436-442.
doi: 10.1016/j.pbi.2008.05.003
[77] Volkov AG ( 2019). Signaling in electrical networks of the Venus flytrap ( Dionaea muscipula Ellis). Bioelectrochemi- stry 125, 25-32.
[78] Wang XM, Devaiah SP, Zhang WH, Welti R ( 2006). Signa- ling functions of phosphatidic acid. Prog Lipid Res 45, 250-278.
doi: 10.1016/j.plipres.2006.01.005
[79] Welti R, Li WQ, Li MY, Sang YM, Biesiada H, Zhou HE, Rajashekar CB, Williams TD, Wang XM ( 2002). Profiling membrane lipids in plant stress responses. Role of pho- spholipase Dα in freezing-induced lipid changes in Ara- bidopsis. J Biol Chem 277, 31994-32002.
doi: 10.1074/jbc.M205375200
[80] Wu LM, Wu HJ, Chen LN, Zhang HY, Gao XW ( 2017). Induction of systemic disease resistance in Nicotiana ben- thamiana by the cyclodipeptides cyclo (L-Pro-L-Pro) and cyclo (D-Pro-D-Pro). Mol Plant Pathol 18, 67-74.
[81] Xia XJ, Zhou YH, Ding J, Shi K, Asami T, Chen ZX, Yu JQ ( 2011). Induction of systemic stress tolerance by brassino- steroid in Cucumis sativus . New Phytol 191, 706-720.
[82] Xia XJ, Zhou YH, Shi K, Zhou J, Foyer CH, Yu JQ ( 2015). Interplay between reactive oxygen species and hormones in the control of plant development and stress tolerance. J Exp Bot 66, 2839-2856.
doi: 10.1093/jxb/erv089
[83] Xu SM, Liao CJ, Jaiswal N, Lee S, Yun DJ, Lee SY, Garvey M, Kaplan I, Mengiste T ( 2018). Tomato PEPR1 ORTHO- LOG RECEPTOR-LIKE KINASE 1 regulates responses to systemin, necrotrophic fungi, and insect herbivory. Plant Cell 30, 2214-2229.
[84] Xuan W, Beeckman T, Xu G ( 2017). Plant nitrogen nutrition: sensing and signaling. Curr Opin Plant Biol 39, 57-65.
doi: 10.1016/j.pbi.2017.05.010
[85] Yan L, Zhai Q, Wei J, Li S, Wang B, Huang T, Du M, Sun J, Kang L, Li CB, Li C ( 2013). Role of tomato lipoxygenase D in wound-induced jasmonate biosynthesis and plant immunity to insect herbivores. PLoS Genet 9, e1003964.
doi: 10.1371/journal.pgen.1003964
[86] Yoo BC, Kragler F, Varkonyi-Gasic E, Haywood V, Archer- Evans S, Lee YM, Lough TJ, Lucas WJ ( 2004). A systemic small RNA signaling system in plants. Plant Cell 16, 1979-2000.
doi: 10.1105/tpc.104.023614
[87] Yuan HM, Liu WC, Lu YT ( 2017). CATALASE2 coordinates SA-mediated repression of both auxin accumulation and JA biosynthesis in plant defenses. Cell Host Microbe 21, 143-155.
doi: 10.1016/j.chom.2017.01.007
[88] Zandalinas SI, Mittler R ( 2018). ROS-induced ROS release in plant and animal cells. Free Radic Biol Med 122, 21-27.
doi: 10.1016/j.freeradbiomed.2017.11.028
[89] Zhang HY, Hu YY ( 2017). Long-distance transport of pro- systemin messenger RNA in tomato. Front Plant Sci 8, 1894.
doi: 10.3389/fpls.2017.01894
[90] Zhang HY, Yu PL, Zhao JH, Jiang HL, Wang HY, Zhu YF, Botella MA, Šamaj J, Li CY, Lin JX ( 2018). Expression of tomato prosystemin gene in Arabidopsis reveals systemic translocation of its mRNA and confers necrotrophic fungal resistance. New Phytol 217, 799-812.
doi: 10.1111/nph.14858
[91] Zhu JK ( 2016). Abiotic stress signaling and responses in plants. Cell 167, 313-324.
doi: 10.1016/j.cell.2016.08.029
[1] . Response of Arabidopsis AtR8 lncRNA to Salt Stress and Its Regulation on Seed Germination [J]. Chin Bull Bot, 2020, 55(4): 0-0.
[2] qi yijunyijun. Small RNA, No Small Feat - Plants deploy 22 nt siRNAs to combat environmental stresses [J]. Chin Bull Bot, 2020, 55(3): 0-0.
[3] Cao Dongdong,Chen Shanyu,Qin Yebo,Wu Huaping,Ruan Guanhai,Huang Yutao. Regulatory Mechanism of Salicylic Acid on Seed Germination Under Salt Stress in Kale [J]. Chin Bull Bot, 2020, 55(1): 49-61.
[4] Luo Jiao,Li Yuting,Zhang Zishan,Che Xingkai,Liang Ying,Li Yuenan,Li Ying,Zhao Shijie,Gao Huiyuan. Effects of the Respiratory Electron Transport Pathways in Relieving Photoinhibition of Chloroplast PSII in Tobacco Leaves [J]. Chin Bull Bot, 2020, 55(1): 31-37.
[5] Yan Zeng,Jie Zhou,Qi Dong,Xiaoge Ping,Zhigang Jiang. Control international trade in wildlife and protect the earth’s biodiversity—Commentary on the 18 th Conference of the Parties of CITES [J]. Biodiv Sci, 2019, 27(9): 1041-1045.
[6] Jun Liu, Ning Wang, Daizong Cui, Lei Lu, Min Zhao. Diversity of bacterial resources in the Greater and Lesser Khinggan Mountains [J]. Biodiv Sci, 2019, 27(8): 903-910.
[7] Zhang Yuanyuan. China’s strategy for incorporating traditional knowledge associated with biodiversity into international multi-lateral agreements [J]. Biodiv Sci, 2019, 27(7): 708-715.
[8] Zhang Xue, Li Xing’an, Su Qinzhi, Cao Qina, Li Chenyi, Niu Qingsheng, Zheng Hao. A curated 16S rRNA reference database for the classification of honeybee and bumblebee gut microbiota [J]. Biodiv Sci, 2019, 27(5): 557-566.
[9] Zhang Shuo, Wu Changyin. Long Noncoding RNA Ef-cd Promotes Maturity Without Yield Penalty in Rice [J]. Chin Bull Bot, 2019, 54(5): 550-553.
[10] Xu Yakun, Ma Yue, Hu Xiaoxi, Wang Jun. Analysis of prospective microbiology research using third-generation sequencing technology [J]. Biodiv Sci, 2019, 27(5): 534-542.
[11] Zhao Yang,Wen Yuanyuan. Development of Convention on Biological Diversity’s Global Platform for Business & Biodiversity: Policy suggestion for China [J]. Biodiv Sci, 2019, 27(3): 339-346.
[12] JIANG Yu-Ling, CHEN Xu-Hui, MIAO Qing, QU Bo. Difference in fungal communities between in roots and in root-associated soil of nine orchids in Liaoning, China [J]. Chin J Plant Ecol, 2019, 43(12): 1079-1090.
[13] Guohua Zhao, Ying Wang, Hui Shang, Xile Zhou, Aihua Wang, Yufeng Li, Hui Wang, Baodong Liu, Yuehong Yan. Ancestral state reconstruction reveals the diversity and evolution of spore ornamentation in Adiantum (Pteridaceae) [J]. Biodiv Sci, 2019, 27(11): 1228-1235.
[14] Xinyu Du, Jinmei Lu, Dezhu Li. Advances in the evolution of plastid genome structure in lycophytes and ferns [J]. Biodiv Sci, 2019, 27(11): 1172-1183.
[15] Zhang Chen,Guo Xin,Weng Sutong,Gao Jun,Fu Jing. Cross-border governance system construction of Qianjiangyuan National Park pilot by referring to the experience of French regional parks [J]. Biodiv Sci, 2019, 27(1): 97-103.
Full text



[1] Hongjuan Jia Junwen Zhang. Quantitative Analysis of Pollen Morphology with MATLAB[J]. Chin Bull Bot, 2007, 24(04): 511 -515 .
[2] Sun Kun and Wang Qing-rui. Cytological Studies on Species of Viola from Northwest China[J]. Chin Bull Bot, 1996, 13(01): 46 -47 .
[3] Pan Rui-chi. Plant growth regulators and rooting[J]. Chin Bull Bot, 1995, 12(专辑3): 8 -14 .
[4] Shumei Ma, Rui Zhang, Yan Sun, Dongjun Liu, Yifan Guo, Wenlin Liu, Fengying Song, Shuping Yang, Jumei Zhang, Guangzu Sun, Hongji Zhang. Genetic Diversity of Wheat Germplasm Resources from Far East Russia and Heilongjiang Province[J]. Chin Bull Bot, 2014, 49(2): 150 -160 .
[5] Cao Kun-fang. An Overview of Plant Reproductive Ecology[J]. Chin Bull Bot, 1993, 10(02): 15 -23 .
[6] WANG Qin YANG Jian WANG Yu-Fei. Pinacecous Cones in the Miocene Shanwang Flora[J]. Chin Bull Bot, 2000, 17(专辑): 262 -263 .
[7] LIU Zhao-Hua Jason Hilton LI Cheng-Sen. Review on the Origin, Evolution and Phylogeny of Marattiles[J]. Chin Bull Bot, 2000, 17(专辑): 39 -52 .
[8] Zheng Zhong-hua. A Method of Preparing Pollen Section for Transmission Electron Microscopy[J]. Chin Bull Bot, 1988, 5(03): 182 -184 .
[9] LIANG Ming-Shan ZENG Yu ZHOU Xiang HOU Liu-Ji LI Xia. Genetic Markers and Their Applications in Identifying Crop Cultivars[J]. Chin Bull Bot, 2001, 18(03): 257 -265 .
[10] Zhang Feng and Shangguan Tie-liang. On the Biomass of Larix principis-rupprechtii Forest in Guandi Mountain , Shanxi Province[J]. Chin Bull Bot, 1992, 9(04): 51 -52 .