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Transcriptomic and physiological analysis reveals interplay between salicylic acid and drought stress in citrus tree floral initiation

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Abstract

Main conclusion

Salicylic acid (SA) and drought stress promote more flowering in sweet orange. The physiological response and molecular mechanism underlying stress-induced floral initiation were discovered by transcriptome profiling. Numerous flowering-regulated genes were identified, and ectopically expressed CsLIP2A promotes early flowering in Arabidopsis.

Abstract

Floral initiation is a critical developmental mechanism associated with external factors, and citrus flowering is mainly regulated by drought stress. However, little is known about the intricate regulatory network involved in stress-induced flowering in citrus. To understand the molecular mechanism of floral initiation in citrus, flower induction was performed on potted Citrus sinensis trees under the combined treatment of salicylic acid (SA) and drought (DR). Physiological analysis revealed that SA treatment significantly normalized the drastic effect of drought stress by increasing antioxidant enzyme activities (SOD, POD, and CAT), relative leaf water content, total chlorophyll, and proline contents and promoting more flowering than drought treatment. Analysis of transcriptome changes in leaves from different treatments showed that 1135, 2728 and 957 differentially expressed genes (DEGs) were revealed in response to DR, SD (SA + DR), and SA (SA + well water) treatments in comparison with the well watered plants, respectively. A total of 2415, 2318 and 1933 DEGs were expressed in DR, SD, and SA in comparison with water recovery, respectively. Some key flowering genes were more highly expressed in SA-treated drought plants than in DR-treated plants. GO enrichment revealed that SA treatment enhances the regulation and growth of meristem activity under drought conditions, but no such a pathway was found to be highly enriched in the control. Furthermore, we focused on various hormones, sugars, starch metabolism, and biosynthesis-related genes. The KEGG analysis demonstrated that DEGs enriched in starch sucrose metabolism and hormonal signal transduction pathways probably account for stress-induced floral initiation in citrus. In addition, a citrus LIPOYLTRANSFERSAE 2A homologous (LIP2A) gene was upregulated by SD treatment. Ectopic expression of CsLIP2A exhibited early flowering in transgenic Arabidopsis. Taken together, this study provides new insight that contributes to citrus tree floral initiation under the SA-drought scenario as well as an excellent reference for stress-induced floral initiation in woody trees.

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Data availability

All data generated or analyzed during this study are included in Supplementary Tables S1–S5 in this published article. The RNA-Seq data from this study have been submitted to the National Center for Biotechnology Information (NCBI) under accession numbers PRJNA741128 [Data release time is June 24, 2022], but are available from the corresponding author on reasonable request.

Abbreviations

DEG:

Differentially expressed genes

DR:

Drought treatment

GO:

Gene ontology

KEGG:

Kyoto Encyclopedia of Genes and Genomes

RWLC:

Relative leaf water content

SA:

Salicylic acid

SD:

SA + DR treatment

WR:

Water recovery

WT:

Well watered

References

  • Abbaspour N, Babaee L (2017) Effect of salicylic acid application on oxidative damage and antioxidant activity of grape (Vitis vinifera L.) under drought stress condition. Int J Hortic Sci Technol 4(1):29–50

    CAS  Google Scholar 

  • Agustí M, Mesejo C, Reig C, Martínez-Fuentes A (2014) Citrus production. In: Dixon GR, Aldous DE (eds) Horticulture: plants for people and places, vol 1. Springer, Dordrecht, pp 159–195

    Google Scholar 

  • Agustí M, Mesejo C, Muñoz-Fambuena N, Vera-Sirera F, de Lucas M, Martínez-Fuentes A, Reig C, Iglesias DJ, Primo-Millo E, Blázquez MA (2020) Fruit-dependent epigenetic regulation of flowering in Citrus. New Phytol 225(1):376–384

    PubMed  Google Scholar 

  • Alabadí D, Blázquez MA, Carbonell J, Ferrándiz C, Pérez-Amador MA (2009) Instructive roles for hormones in plant development. Int J Dev Biol 53(8):1597

    PubMed  Google Scholar 

  • Albrigo G, Chica E (2011) Citrus shoot age and flowering potential. In: 102nd annual meeting of the American society for horticultural science, 2011, pp 56–59

  • Ali B (2017) Salicylic acid induced antioxidant system enhances the tolerence to aluminium in mung bean (Vigna radiata L. Wilczek) plants. Indian J Plant Physiol 22(2):178–189

    CAS  Google Scholar 

  • Ali AG, Lovatt C (1995) Relationship of polyamines to low-temperature stress-induced flowering of the ‘Washington’navel orange (Citrus sinensis L. Osbeck). J Hortic Sci 70(3):491–498

    CAS  Google Scholar 

  • Arias-Sibillotte M, Borges A, Díaz P, Ferenczi A, Severino V (2019) Leaf proline content and its relation to fruit load and flowering in citrus under field conditions. Rev Bras Frutic 41(2):e087

    Google Scholar 

  • Ariizumi T, Hauvermale AL, Nelson SK, Hanada A, Yamaguchi S, Steber CM (2013) Lifting DELLA repression of Arabidopsis seed germination by nonproteolytic gibberellin signaling. Plant Physiol 162(4):2125–2139

    CAS  PubMed  PubMed Central  Google Scholar 

  • Arrom L, Munné-Bosch S (2012) Sucrose accelerates flower opening and delays senescence through a hormonal effect in cut lily flowers. Plant Sci 188–189:41–47. https://doi.org/10.1016/j.plantsci.2012.02.012

    Article  CAS  PubMed  Google Scholar 

  • Ávila C, Guardiola JL, Nebauer SG (2012) Response of the photosynthetic apparatus to a flowering-inductive period by water stress in citrus. Trees 26(3):833–840

    Google Scholar 

  • Aziz A, Kapoor D (2018) Salicylic acid: it’s physiological role and interactions. Res J Pharm Technol 11(7):3171–3177

    Google Scholar 

  • Banday ZZ, Nandi AK (2015) Interconnection between flowering time control and activation of systemic acquired resistance. Front Plant Sci 6:174

    PubMed  PubMed Central  Google Scholar 

  • Barbier F, Péron T, Lecerf M, Perez-Garcia M-D, Barrière Q, Rolčík J, Boutet-Mercey S, Citerne S, Lemoine R, Porcheron B, Roman H, Leduc N, Le Gourrierec J, Bertheloot J, Sakr S (2015) Sucrose is an early modulator of the key hormonal mechanisms controlling bud outgrowth in Rosa hybrida. J Exp Bot 66(9):2569–2582. https://doi.org/10.1093/jxb/erv047

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baron D, Bravo JP, Maia IG, Pina A, Ferreira G (2016) UGP gene expression and UDP-glucose pyrophosphorylase enzymatic activity in grafting annonaceous plants. Acta Physiol Plant 38(3):79

    Google Scholar 

  • Blankenberg D, Gordon A, Von Kuster G, Coraor N, Taylor J, Nekrutenko A, The Galaxy T (2010) Manipulation of FASTQ data with Galaxy. Bioinformatics 26(14):1783–1785. https://doi.org/10.1093/bioinformatics/btq281

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brito C, Dinis L-T, Meijón M, Ferreira H, Pinto G, Moutinho-Pereira J, Correia C (2018) Salicylic acid modulates olive tree physiological and growth responses to drought and rewatering events in a dose dependent manner. J Plant Physiol 230:21–32

    CAS  PubMed  Google Scholar 

  • Cabo S, Aires A, Carvalho R, Vilela A, Pascual-Seva N, Silva AP, Gonçalves B (2021) Kaolin, Ascophyllum nodosum and salicylic acid mitigate effects of summer stress improving hazelnut quality. J Sci Food Agric 101(2):459–475

    CAS  PubMed  Google Scholar 

  • Campos-Rivero G, Osorio-Montalvo P, Sánchez-Borges R, Us-Camas R, Duarte-Aké F, De-la-Peña C (2017) Plant hormone signaling in flowering: an epigenetic point of view. J Plant Physiol 214:16–27

    CAS  PubMed  Google Scholar 

  • Chica EJ, Albrigo LG (2013) Cool temperature and water deficit interact during floral induction in citrus. Proc Fla State Hortic Soc 126:45–50

    Google Scholar 

  • Cho LH, Yoon J, An GJTPJ (2017) The control of flowering time by environmental factors. Plant J 90(4):708–719

    CAS  PubMed  Google Scholar 

  • Chowdhury Z, Mohanty D, Giri MK, Venables BJ, Chaturvedi R, Chao A, Petros RA, Shah J (2020) Dehydroabietinal promotes flowering time and plant defense in Arabidopsis via the autonomous pathway genes FLOWERING LOCUS D, FVE, and RELATIVE OF EARLY FLOWERING 6. J Exp Bot 71(16):4903–4913

    CAS  PubMed  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16(6):735–743

    CAS  PubMed  Google Scholar 

  • Corbesier L, Lejeune P, Bernier G (1998) The role of carbohydrates in the induction of flowering in Arabidopsis thaliana: comparison between the wild type and a starchless mutant. Planta 206(1):131–137

    CAS  PubMed  Google Scholar 

  • Corbesier L, Vincent C, Jang S, Fornara F, Fan Q, Searle I, Giakountis A, Farrona S, Gissot L, Turnbull C (2007) FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Science 316(5827):1030–1033

    CAS  PubMed  Google Scholar 

  • Damalas CA (2019) Improving drought tolerance in sweet basil (Ocimum basilicum) with salicylic acid. Sci Hortic 246:360–365

    CAS  Google Scholar 

  • Dubois A, Remay A, Raymond O, Balzergue S, Chauvet A, Maene M, Pécrix Y, Yang S-H, Jeauffre J, Thouroude T (2011) Genomic approach to study floral development genes in Rosa sp. PLoS ONE 6(12):e28455

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wilmowicz E, Kesy J, Kopcewicz J (2008) Ethylene and aba interactions in the regulation of flower induction in pharbitis nil. J Plant Physiol 165(18):1917–1928

    CAS  PubMed  Google Scholar 

  • Endo T, Shimada T, Nakata Y, Fujii H, Matsumoto H, Nakajima N, Ikoma Y, Omura M (2018) Abscisic acid affects expression of citrus FT homologs upon floral induction by low temperature in Satsuma mandarin (Citrus unshiu Marc.). Tree Physiol 38(5):755–771

    CAS  PubMed  Google Scholar 

  • Eom SH, Baek S-A, Kim JK, Hyun TK (2018) Transcriptome analysis in Chinese cabbage (Brassica rapa ssp. pekinensis) provides the role of glucosinolate metabolism in response to drought stress. Molecules 23(5):1186

    PubMed Central  Google Scholar 

  • Fan Z, Li J, Li X, Wu B, Wang J, Liu Z, Yin H (2015) Genome-wide transcriptome profiling provides insights into floral bud development of summer-flowering Camellia azalea. Sci Rep 5(1):1–11

    CAS  Google Scholar 

  • Fornara F, de Montaigu A, Coupland G (2010) SnapShot: control of flowering in Arabidopsis. Cell 141(3):550

    PubMed  Google Scholar 

  • Fu L, Tan D, Sun X, Ding Z, Zhang J (2020) Transcriptional analysis reveals potential genes and regulatory networks involved in salicylic acid-induced flowering in duckweed (Lemna gibba). Plant Physiol Biochem 155:512–522

    CAS  PubMed  Google Scholar 

  • González L, González-Vilar M (2001) Determination of relative water content. In: Reigosa Roger MJ (ed) Handbook of plant ecophysiology techniques. Springer, Dordrecht, pp 207–212

    Google Scholar 

  • Hayat S, Hasan SA, Fariduddin Q, Ahmad A (2008) Growth of tomato (Lycopersicon esculentum) in response to salicylic acid under water stress. J Plant Interact 3(4):297–304

    CAS  Google Scholar 

  • Hayat Q, Hayat S, Irfan M, Ahmad A (2010) Effect of exogenous salicylic acid under changing environment: a review. Environ Exp Bot 68(1):14–25

    CAS  Google Scholar 

  • Honma T, Goto K (2001) Complexes of MADS-box proteins are sufficient to convert leaves into floral organs. Nature 409(6819):525–529. https://doi.org/10.1038/35054083

    Article  CAS  PubMed  Google Scholar 

  • Huang AHC (1996) Oleosins and oil bodies in seeds and other organs. Plant Physiol 110(4):1055–1061. https://doi.org/10.1104/pp.110.4.1055

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hui W, Yang Y, Wu G, Peng C, Chen X, Zayed MZ (2017) Transcriptome profile analysis reveals the regulation mechanism of floral sex differentiation in Jatropha curcas L. Sci Rep 7(1):1–13

    Google Scholar 

  • Jambunathan N (2010) Determination and detection of reactive oxygen species (ROS), lipid peroxidation, and electrolyte leakage in plants. In: Sunkar R (ed) Plant stress tolerance. Springer, pp 291–297

    Google Scholar 

  • Jesus C, Meijon M, Monteiro P, Correia B, Amaral J, Escandon M, Canal MJ, Pinto G (2015) Salicylic acid application modulates physiological and hormonal changes in Eucalyptus globulus under water deficit. Environ Exp Bot 118:56–66

    CAS  Google Scholar 

  • Kazan K, Lyons R (2015) The link between flowering time and stress tolerance. J Exp Bot 67(1):47–60

    PubMed  Google Scholar 

  • Kim HU, Hsieh K, Ratnayake C, Huang AHC (2002) A novel group of oleosins is present inside the pollen of Arabidopsis. J Biol Chem 277(25):22677–22684

    CAS  PubMed  Google Scholar 

  • Klepikova AV, Logacheva MD, Dmitriev SE, Penin AA (2015) RNA-seq analysis of an apical meristem time series reveals a critical point in Arabidopsis thaliana flower initiation. BMC Genom 16(1):16

    Google Scholar 

  • Klessig DF, Tian M, Choi HW (2016) Multiple targets of salicylic acid and its derivatives in plants and animals. Frontiers Immunol 7:206

    Google Scholar 

  • Koo YM, Heo AY, Choi HW (2020) Salicylic acid as a safe plant protector and growth regulator. Plant Pathol J 36(1):1–10

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kordi S, Saidi M, Ghanbari F (2013) Induction of drought tolerance in sweet basil (Ocimum basilicum L.) by salicylic acid. Int J Agric Food Res 2(2):18–26

    Google Scholar 

  • Koshita Y, Takahara T (2004) Effect of water stress on flower-bud formation and plant hormone content of satsuma mandarin (Citrus unshiu Marc.). Sci Hortic 99(3–4):301–307

    CAS  Google Scholar 

  • Kruger NJ (2009) The Bradford method for protein quantitation. In: Walker JM (ed) The protein protocols handbook. Springer, Berlin, pp 17–24

    Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33(7):1870–1874. https://doi.org/10.1093/molbev/msw054

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Laxa M, Liebthal M, Telman W, Chibani K, Dietz K-J (2019) The role of the plant antioxidant system in drought tolerance. Antioxidants 8(4):94

    CAS  PubMed Central  Google Scholar 

  • Lévesque-Lemay M, Chabot D, Hubbard K, Chan JK, Miller S, Robert LS (2016) Tapetal oleosins play an essential role in tapetosome formation and protein relocation to the pollen coat. New Phytol 209(2):691–704

    PubMed  Google Scholar 

  • Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 25(14):1754–1760. https://doi.org/10.1093/bioinformatics/btp324

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li J-X, Hou X-J, Zhu J, Zhou J-J, Huang H-B, Yue J-Q, Gao J-Y, Du Y-X, Hu C-X, Hu C-G (2017) Identification of genes associated with lemon floral transition and flower development during floral inductive water deficits: a hypothetical model. Front Plant Sci 8:1013

    PubMed  PubMed Central  Google Scholar 

  • Li Y, Zhang D, An N, Fan S, Zuo X, Zhang X, Zhang L, Gao C, Han M, Xing L (2019) Transcriptomic analysis reveals the regulatory module of apple (Malus × domestica) floral transition in response to 6-BA. BMC Plant Biol 19(1):1–17

    Google Scholar 

  • Liu K, Feng S, Pan Y, Zhong J, Chen Y, Yuan C, Li H (2016) Transcriptome analysis and identification of genes associated with floral transition and flower development in sugar apple (Annona squamosa L.). Front Plant Sci 7:1695

    PubMed  PubMed Central  Google Scholar 

  • Liu F, Wang Y, Ding Z, Zhao L, Xiao J, Wang L, Ding S (2017) Transcriptomic analysis of flower development in tea (Camellia sinensis (L.)). Gene 631:39–51

    CAS  PubMed  Google Scholar 

  • Manzi M, Borsani O, Díaz P, Rivas F (2015) Relationship between flower intensity, oxidative damage and protection in Citrus under water stress conditions. Acta Hortic 1065:1243–1249. https://doi.org/10.17660/ActaHortic.2015.1065.158

    Article  Google Scholar 

  • Mao X, Cai T, Olyarchuk JG, Wei L (2005) Automated genome annotation and pathway identification using the KEGG Orthology (KO) as a controlled vocabulary. Bioinformatics 21(19):3787–3793. https://doi.org/10.1093/bioinformatics/bti430

    Article  CAS  PubMed  Google Scholar 

  • Martignago D, Siemiatkowska B, Lombardi A, Conti L (2020) Abscisic acid and flowering regulation: many targets, different places. Int J Mol Sci. https://doi.org/10.3390/ijms21249700

    Article  PubMed  PubMed Central  Google Scholar 

  • Martínez C, Pons E, Prats G, León J (2004) Salicylic acid regulates flowering time and links defence responses and reproductive development. Plant J 37(2):209–217

    PubMed  Google Scholar 

  • Martín-Mex R, Nexticapan-Garcéz Á, Villanueva-Couoh E, Uicab-Quijano V, Vergara-Yoisura S, Larqué-Saavedra A (2015) Salicylic acid stimulates flowering in micropopagated gloxinia plants. Rev Fitotec Mex 38(2):115–118

    Google Scholar 

  • Mesejo C, Marzal A, Martínez-Fuentes A, Reig C, de Lucas M, Iglesias DJ, Primo-Millo E, Blázquez MA, Agustí M (2021) Reversion of fruit-dependent inhibition of flowering in Citrus requires sprouting of buds with epigenetically silenced CcMADS19. New Phytol. https://doi.org/10.1111/nph.17681

    Article  PubMed  Google Scholar 

  • Mishra P, Panigrahi KC (2015) GIGANTEA–an emerging story. Front Plant Sci 6:8

    PubMed  PubMed Central  Google Scholar 

  • Mizoguchi T, Wright L, Fujiwara S, Cremer F, Lee K, Onouchi H, Mouradov A, Fowler S, Kamada H, Putterill J (2005) Distinct roles of GIGANTEA in promoting flowering and regulating circadian rhythms in Arabidopsis. Plant Cell 17(8):2255–2270

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mohammadi H, Imani A, Asghari M, Talaie A (2020) Exogenous salicylic acid mitigates adverse effects of salinity on some photosynthesis-related parameters of almond. J Agric Sci Technol 22(2):519–534

    Google Scholar 

  • Munoz-Fambuena N, Mesejo C, González-Mas MC, Iglesias DJ, Primo-Millo E, Agustí M (2012) Gibberellic acid reduces flowering intensity in sweet orange [Citrus sinensis (L.) Osbeck] by repressing CiFT gene expression. J Plant Growth Regul 31(4):529–536

    CAS  Google Scholar 

  • Najafabadi MY, Ehsanzadeh P (2017) Photosynthetic and antioxidative upregulation in drought-stressed sesame (Sesamum indicum L.) subjected to foliar-applied salicylic acid. Photosynthetica 55(4):611–622

    Google Scholar 

  • Nakamura Y, Andrés F, Kanehara K, Liu Y-C, Dörmann P, Coupland G (2014) Arabidopsis florigen FT binds to diurnally oscillating phospholipids that accelerate flowering. Nat Commun 5:3553. https://doi.org/10.1038/ncomms4553

    Article  CAS  PubMed  Google Scholar 

  • Nakashima A, von Reuss SH, Tasaka H, Nomura M, Mochizuki S, Iijima Y, Aoki K, Shibata D, Boland W, Takabayashi J, Matsui K (2013) Traumatin- and dinortraumatin-containing galactolipids in Arabidopsis: their formation in tissue-disrupted leaves as counterparts of green leaf volatiles. J Biol Chem 288(36):26078–26088. https://doi.org/10.1074/jbc.M113.487959

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nazar R, Umar S, Khan N, Sareer O (2015) Salicylic acid supplementation improves photosynthesis and growth in mustard through changes in proline accumulation and ethylene formation under drought stress. S Afr J Bot 98:84–94

    CAS  Google Scholar 

  • Parthibane V, Rajakumari S, Venkateshwari V, Iyappan R, Rajasekharan R (2012) Oleosin is bifunctional enzyme that has both monoacylglycerol acyltransferase and phospholipase activities. J Biol Chem 287(3):1946–1954

    CAS  PubMed  Google Scholar 

  • Patni B, Ansari S (2019) Role of exogenous application of salicylic acid on medicinal plants under drought stress: a review. J Stress Physiol Biochem 15(4):76–85

    CAS  Google Scholar 

  • Pérez-Pérez J, Syvertsen JP, Botía P, García-Sánchez F (2007) Leaf water relations and net gas exchange responses of salinized Carrizo citrange seedlings during drought stress and recovery. Ann Bot 100(2):335–345

    PubMed  PubMed Central  Google Scholar 

  • Poschet G, Hannich B, Raab S, Jungkunz I, Klemens PA, Krueger S, Wic S, Neuhaus HE, Büttner M (2011) A novel Arabidopsis vacuolar glucose exporter is involved in cellular sugar homeostasis and affects the composition of seed storage compounds. Plant Physiol 157(4):1664–1676

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rivas-San Vicente M, Plasencia J (2011) Salicylic acid beyond defence: its role in plant growth and development. J Exp Bot 62(10):3321–3338

    CAS  PubMed  Google Scholar 

  • Saito T, Wang S, Ohkawa K, Ohara H, Ikeura H, Ogawa Y, Kondo S (2017) Lipid droplet-associated gene expression and chromatin remodelling in LIPASE 5’-upstream region from beginning-to mid-endodormant bud in “Fuji” apple. Plant Mol Biol 95(4):441–449

    CAS  PubMed  Google Scholar 

  • Sakamoto D, Nakamura Y, Sugiura H, Sugiura T, Asakura T, Yokoyama M, Moriguchi T (2010) Effect of 9-hydroxy-10-oxo-12 (Z), 15 (Z)-octadecadienoic acid (KODA) on endodormancy breaking in flower buds of Japanese pear. HortScience 45(10):1470–1474

    Google Scholar 

  • Seyfferth C, Tsuda K (2014) Salicylic acid signal transduction: the initiation of biosynthesis, perception and transcriptional reprogramming. Front Plant Sci 5:697

    PubMed  PubMed Central  Google Scholar 

  • Shafique Khan F, Zeng R-F, Gan Z-M, Zhang J-Z, Hu C-G (2021) Genome-wide identification and expression profiling of the WOX gene family in Citrus sinensis and functional analysis of a CsWUS member. Int J Mol Sci 22(9):4919

    PubMed  PubMed Central  Google Scholar 

  • Shah K, An N, Kamanova S, Chen L, Jia P, Zhang C, Mobeen Tahir M, Han M, Ding Y, Ren X, Xing L (2021) Regulation of flowering time by improving leaf health markers and expansion by salicylic acid treatment: a new approach to induce flowering in malus domestica. Front Plant Sci 12. https://doi.org/10.3389/fpls.2021.655974

    Article  PubMed  PubMed Central  Google Scholar 

  • Shalom L, Samuels S, Zur N, Shlizerman L, Zemach H, Weissberg M, Ophir R, Blumwald E, Sadka A (2012) Alternate bearing in citrus: changes in the expression of flowering control genes and in global gene expression in on-versus off-crop trees. PLoS ONE 7(10):e46930

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shen J, Xiao Q, Qiu H, Chen C, Chen H (2016) Integrative effect of drought and low temperature on litchi (Litchi chinensis Sonn.) floral initiation revealed by dynamic genome-wide transcriptome analysis. Sci Rep 6:32005. https://doi.org/10.1038/srep32005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shimakawa A, Shiraya T, Ishizuka Y, Wada KC, Mitsui T, Takeno K (2012) Salicylic acid is involved in the regulation of starvation stress-induced flowering in Lemna paucicostata. J Plant Physiol 169(10):987–991

    CAS  PubMed  Google Scholar 

  • Siloto RM, Findlay K, Lopez-Villalobos A, Yeung EC, Nykiforuk CL, Moloney MM (2006) The accumulation of oleosins determines the size of seed oilbodies in Arabidopsis. Plant Cell 18(8):1961–1974

    CAS  PubMed  PubMed Central  Google Scholar 

  • Skm AE-N, Abdelkhalek A, Baiea M, Amin O (2020) Response of valencia orange trees grown under sandy soil to mitigation of heat stress by melatonin, gibberellin and salicylic acid application. Plant Arch 20(2):2252–2258

    Google Scholar 

  • Song K, Kim HC, Shin S, Kim K-H, Moon J-C, Kim JY, Lee B-M (2017) Transcriptome analysis of flowering time genes under drought stress in maize leaves. Front Plant Sci 8:267

    PubMed  PubMed Central  Google Scholar 

  • Susila H, Juric S, Liu L, Gawarecka K, Chung KS, Jin S, Kim S-J, Nasim Z, Youn G, Suh MC, Yu H, Ahn JH (2021) Florigen sequestration in cellular membranes modulates temperature-responsive flowering. Science 373(6559):1137–1141. https://doi.org/10.1126/science.abh4054

    Article  CAS  PubMed  Google Scholar 

  • Tang Y, Sun X, Wen T, Liu M, Yang M, Chen X (2017) Implications of terminal oxidase function in regulation of salicylic acid on soybean seedling photosynthetic performance under water stress. Plant Physiol Biochem 112:19–28

    CAS  PubMed  Google Scholar 

  • Tarazona S, Furio-Tari P, Turra D, Di Pietro A, Jose Nueda M, Ferrer A, Conesa A (2015) Data quality aware analysis of differential expression in RNA-seq with NOISeq R/Bioc package. Nucleic Acids Res 43(21):e140. https://doi.org/10.1093/nar/gkv711

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • van Dijken AJ, Schluepmann H, Smeekens SC (2004) Arabidopsis trehalose-6-phosphate synthase 1 is essential for normal vegetative growth and transition to flowering. Plant Physiol 135(2):969–977

    PubMed  PubMed Central  Google Scholar 

  • Veerabagu M, Paul KL, Rinne PL, van der Schoot C (2020) Plant lipid bodies traffic on actin to plasmodesmata motorized by myosin XIs. Int J Mol Sci 21(4):1422

    CAS  PubMed Central  Google Scholar 

  • Wada KC, Takeno K (2010) Stress-induced flowering plant. Signal Behav 5(8):944–947

    Google Scholar 

  • Wada KC, Yamada M, Shiraya T, Takeno K (2010) Salicylic acid and the flowering gene FLOWERING LOCUS T homolog are involved in poor-nutrition stress-induced flowering of Pharbitis nil. J Plant Physiol 167(6):447–452

    CAS  PubMed  Google Scholar 

  • Wang C-Y, Chiou C-Y, Wang H-L, Krishnamurthy R, Venkatagiri S, Tan J, Yeh K-W (2008) Carbohydrate mobilization and gene regulatory profile in the pseudobulb of Oncidium orchid during the flowering process. Planta 227(5):1063–1077

    CAS  PubMed  Google Scholar 

  • Wani AB, Chadar H, Wani AH, Singh S, Upadhyay N (2017) Salicylic acid to decrease plant stress. Environ Chem Lett 15(1):101–123

    CAS  Google Scholar 

  • Wilson RN, Heckman JW, Somerville CR (1992) Gibberellin is required for flowering in Arabidopsis thaliana under short days. Plant Physiol 100(1):403–408

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wong CE, Singh MB, Bhalla PL (2013) The dynamics of soybean leaf and shoot apical meristem transcriptome undergoing floral initiation process. PLoS ONE 8(6):e65319

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wu Y, Zhang D, Chu JY, Boyle P, Wang Y, Brindle ID, De Luca V, Després C (2012) The Arabidopsis NPR1 protein is a receptor for the plant defense hormone salicylic acid. Cell Rep 1(6):639–647

    CAS  PubMed  Google Scholar 

  • Wu P, Wu C, Zhou B (2017) Drought stress induces flowering and enhances carbohydrate accumulation in Averrhoa Carambola. Hortic Plant J 3(2):60–66

    Google Scholar 

  • Xia Y, Xue B, Shi M, Zhan F, Wu D, Jing D, Wang S, Guo Q, Liang G, He Q (2020) Comparative transcriptome analysis of flower bud transition and functional characterization of EjAGL17 involved in regulating floral initiation in loquat. PLoS ONE 15(10):e0239382

    CAS  PubMed  PubMed Central  Google Scholar 

  • Xie S, Xiaoli Z, Lu X, Huang C, Xiao Y, Li J (2016) Effect of water stress on citrus physiological characteristics, jasmine acid biosynthesis and correlative gene expression. Acta Hortic 1112:247–254. https://doi.org/10.17660/ActaHortic.2016.1112.34

    Article  Google Scholar 

  • Xing L-B, Zhang D, Li Y-M, Shen Y-W, Zhao C-P, Ma J-J, An N, Han M-Y (2015) Transcription profiles reveal sugar and hormone signaling pathways mediating flower induction in apple (Malus domestica Borkh.). Plant Cell Physiol 56(10):2052–2068

    CAS  PubMed  Google Scholar 

  • Xu Q, Chen L-L, Ruan X, Chen D, Zhu A, Chen C, Bertrand D, Jiao W-B, Hao B-H, Lyon MP, Chen J, Gao S, Xing F, Lan H, Chang J-W, Ge X, Lei Y, Hu Q, Miao Y, Wang L, Xiao S, Biswas MK, Zeng W, Guo F, Cao H, Yang X, Xu X-W, Cheng Y-J, Xu J, Liu J-H, Luo OJ, Tang Z, Guo W-W, Kuang H, Zhang H-Y, Roose ML, Nagarajan N, Deng X-X, Ruan Y (2013) The draft genome of sweet orange (Citrus sinensis). Nat Genet 45(1):59–66. https://doi.org/10.1038/ng.2472

    Article  CAS  PubMed  Google Scholar 

  • Yamada M, Takeno K (2014) Stress and salicylic acid induce the expression of PnFT2 in the regulation of the stress-induced flowering of Pharbitis nil. J Plant Physiol 171(3–4):205–212

    CAS  PubMed  Google Scholar 

  • Yamaguchi A, Wu M-F, Yang L, Wu G, Poethig RS, Wagner D (2009) The microRNA-regulated SBP-box transcription factor SPL3 is a direct upstream activator of LEAFY, FRUITFULL, and APETALA1. Dev Cell 17(2):268–278

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yang A, Smyth H, Chaliha M, James A (2016) Sensory quality of soymilk and tofu from soybeans lacking lipoxygenases. Food Sci Nutr 4(2):207–215

    CAS  PubMed  Google Scholar 

  • Yusuf M, Hayat S, Alyemeni MN, Fariduddin Q, Ahmad A (2013) Salicylic acid: physiological roles in plants. In: Hayat S, Ahmad A, Nasser Alyemeni M (eds) Salicylic acid: plant, growth and development. Springer, Berlin, pp 15–30

    Google Scholar 

  • Zhang Y, Li X (2019) Salicylic acid: biosynthesis, perception, and contributions to plant immunity. Curr Opin Plant Biol 50:29–36

    CAS  PubMed  Google Scholar 

  • Zhang H-N, Wei Y-Z, Shen J-Y, Lai B, Huang X-M, Ding F, Su Z-X, Chen H-B (2014) Transcriptomic analysis of floral initiation in litchi (Litchi chinensis Sonn.) based on de novo RNA sequencing. Plant Cell Rep 33(10):1723–1735

    CAS  PubMed  Google Scholar 

  • Zhang H, Shen J, Wei Y, Chen H (2017) Transcriptome profiling of litchi leaves in response to low temperature reveals candidate regulatory genes and key metabolic events during floral induction. BMC Genom 18:363

    Google Scholar 

  • Zhao D, Zhang X, Fang Z, Wu Y, Tao J (2019) Physiological and transcriptomic analysis of tree peony (Paeonia section Moutan DC.) in response to drought stress. Forests 10(2):135. https://doi.org/10.3390/f10020135

    Article  Google Scholar 

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Acknowledgements

This research was supported financially by the National Major Research and Development Plan (2018YFD100004), the National Natural Science Foundation of China (Grant nos. 31972356, 31772252, 31601743, and 31872045).

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  1. Faiza Shafique Khan and Zhi-Meng Gan contributed equally to this paper.

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  1. Key Laboratory of Horticultural Plant Biology (Ministry of Education), College of Horticulture and Forestry Science, Huazhong Agricultural University, Wuhan, 430070, China

    Faiza Shafique Khan, Zhi-Meng Gan, En-Qing Li, Meng-Ke Ren, Chun-Gen Hu & Jin-Zhi Zhang

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  1. Faiza Shafique Khan
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Khan, F.S., Gan, ZM., Li, EQ. et al. Transcriptomic and physiological analysis reveals interplay between salicylic acid and drought stress in citrus tree floral initiation. Planta 255, 24 (2022). https://doi.org/10.1007/s00425-021-03801-2

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