Abstract
Abscisic acid (ABA) regulates plant growth and development, but the role of ABA in the development of reproductive organs in tomato has rarely been addressed. In the present study, the role of ABA in the regulation of male and female gametogenesis as well as pollen development and germination is tested in tomato. qRT-PCR and in situ hybridization analysis of 9-cis-epoxycarotenoid dioxygenase (SlNCED1), a key enzyme in the ABA biosynthetic pathway, showed high expression of SlNCED1 primarily in the meristem during gametogenesis and mainly in ovule, stigma, anther/pollen and vascular tissues during floral organ development. SlNCED1 expression and ABA accumulation in anther peak at stages 13–14, suggesting that ABA plays a role in the primary formation of pollen grains. Over expression and suppression of SlNCED1 led to the abnormal development of anther/pollen, especially in SlNCED1-OE lines, which have serious pollen deterioration. The percentage of pollen germination in wild type is 91.47%, whereas it is 6.85% in OE transgenic lines and 38.4% at anthesis in RNAi lines. RNA-Seq of anthers shows that SlNCED1-OE can significantly enhance the expression of SlPP2Cs and down-regulate the expression of SlMYB108 and SlMYB21, which are anther/flower-specific transcriptional factors in tomato. Finally, anther transcriptome data indicate that SlNCED1 is involved in ABA-mediated regulation in pollen/anther metabolism, cell wall modification, and transcription levels. These results support an important role for ABA in the development of reproductive organs in tomato and contribute to the elucidation of the underlying regulatory mechanisms.
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References
Himmelbach A, Yang Y, Grill E (2003) Relay and control of abscisic acid signaling. Curr Opin Plant Biol 6(5):470–479
Wang ZY, Xiong L, Li W, Zhu JK, Zhu J (2011) The plant cuticle is required for osmotic stress regulation of abscisic acid biosynthesis and osmotic stress tolerance in arabidopsis. Plant Cell 23(5):1971–1984
Wasilewska A, Vlad F, Sirichandra C, Redko Y, Jammes F, Valon C, dit Frey NF, Leung J (2008) An update on abscisic acid signaling in plants and more. Mol Plant 1(2):198–217
Chernys JT, Zeevaart JAD (2000) Characterization of the 9-cis-epoxycarotenoid dioxygenase gene family and the regulation of abscisic acid biosynthesis in avocado. Plant Physiol 124(1):343–353
Finkelstein R (2013) Abscisic acid synthesis and response. Arabidopsis Book 11:e0166
Wilkinson S, Davies WJ (2002) ABA-based chemical signalling: the co-ordination of responses to stress in plants. Plant Cell Environ 25:195–210
Hauser F, Waadt R, Schroeder JI (2011) Evolution of abscisic acid synthesis and signaling mechanisms. Curr Biol 21(9):R346–R355
Nambara E, Marion-Poll A (2005) Abscisic acid biosynthesis and catabolism. Annu Rev Plant Biol 56:165–185
Qin XQ, Zeevaart JAD (1999) The 9-cis-epoxycarotenoid cleavage reaction is the key regulatory step of abscisic acid biosynthesis in water-stressed bean. Proc Natl Acad Sci USA 96:15354–15361
Lee KH, Piao HL, Kim HY, Choi SM, Jiang F, Hartung W, Hwang I, Kwak JM, Lee IJ, Hwang I (2006) Activation of glucosidase via stress-induced polymerization rapidly increases active pools of abscisic acid. Cell 126(6):1109–1120
Xu ZY, Lee KH, Dong T, Jeong JC, Jin JB, Kanno Y, Kim DH, Kim SY, Seo M, Bressan RA, Yun DJ, Inhwan Hwang I (2012) A vacuolar β-glucosidase homolog that possesses glucose-conjugated abscisic acid hydrolyzing activity plays an important role in osmotic stress responses in Arabidopsis. Plant Cell 24:2184–2199
Cutler AJ, Krochko JE (1999) Formation and breakdown of ABA. Trends Plant Sci 4:472–478
Kushiro T, Okamoto M, Nakabayashi K, Yamagishi K, Kitamura S, Asami T, Hirai N, Koshiba T, Kamiya Y, Nambara E (2004) The Arabidopsis cytochrome P450 CYP707A encodes ABA 8-hydroxylases: key enzymes in ABA catabolism. EMBO J 23:1647–1656
Okamoto M, Kuwahara A, Seo M, Kushiro T, Asami T, Hirai N, Kamiya Y, Koshiba T, Nambara E (2006) CYP707A1 and CYP707A2, which encode abscisic acid 8′-hydroxylases, are indispensable for proper control of seed dormancy and germination in arabidopsis. Physiol Plant 141:97–107
Priest DM, Ambrose SJ, FánE Vaistij, Elias L, Higgins GS, Ross ARS, Abrams SR, Bowles DJ (2006) Use of the glucosyltransferase UGT71B6 to disturb abscisic acid homeostasis in Arabidopsis thaliana. Plant J 46(3):492–502
Ross J, O’Neill D (2001) New interactions between classical plant hormones. Trends Plant Sci 6:2–4
Sun Y, Ji K, Liang B, Du Y, Jiang L, Wang J, Kai W, Zhang Y, Zhai X, Chen P, Wang H, Leng P (2017) Suppressing ABA uridine diphosphate glucosyltransferase (SlUGT75C1) alters fruit ripening and the stress response in tomato. Plant J 91(4):574–589
Buesa C, Dominguez M, Vendrell M (1994) Abscisic-acid effects on ethylene production and respiration rate in detached apple fruits at different stages of development. Revista Espanola de Ciencia y Tecnologia de Alimentos 34(5):495–506
Zhang M, Yuan B, Leng P (2009) The role of ABA in triggering ethylene biosynthesis and ripening of tomato fruit. J Exp Bot 60(6):1579–1588
Kojima K, Yamada Y, Yamamoto M (1995) Effects of abscisic-acid injection on sugar and organic-acid contents of citrus-fruit. J Jpn Soc Hortic Sci 64(1):17–21
Kondo S, Inoue K (1997) Abscisic acid (ABA) and 1-aminocyclopropane-1-carboxylic acid (ACC) content during growth of Satohnishiki cherry fruit, and the effect of ABA and ethephon application on fruit quality. J Hortic Sci 72(2):221–227
Ji K, Kai W, Zhao B, Sun Y, Yuan B, Dai S, Li Q, Chen P, Wang Y, Pei Y, Wang H, Guo Y, Leng P (2014) SlNCED1 and SlCYP707A2: key genes involved in ABA metabolism during tomato fruit ripening. J Exp Bot 65(18):5243–5255
Zhang M, Leng P, Zhang G, Li X (2009) Cloning and functional analysis of 9-cis-epoxycarotenoid dioxygenase (NCED) genes encoding a key enzyme during abscisic acid biosynthesis from peach and grape fruits. J Plant Physiol 166:1241–1252
Sun L, Sun Y, Zhang M, Wang L, Ren J, Cui M, Wang Y, Ji K, Li P, Li Q, Chen P, Dai S, Duan C, Wu Y, Leng P (2012) Suppression of 9-cis-epoxycarotenoid dioxygenase, which encodes a key enzyme in abscisic acid biosynthesis, alters fruit texture in transenic tomato. Plant Physiol 158(1):283–298
Sun L, Yuan B, Zhang M, Wang L, Cui M, Wang Q, Leng P (2012) Fruit-specific RNAi-mediated suppression of SlNCED1 increases both lycopene and β-carotene contents in tomato fruit. J Exp Bot 63(8):3097–3108
Galpaz N, Wang Q, Menda N, Zamir D, Hirschberg JP (2008) Abscisic acid deficiency in the tomato mutant high-pigment 3 leading to increased plastid number and higher fruit lycopene content. Plant J 53:717–730
Taylor IB, Burbidge A, Thompson AJ (2000) Control of abscisic acid synthesis. J Exp Bot 51(350):1563–1574
Nicolas P, Lecourieux D, Kappel C, Cluzet S, Cramer G, Delrot S, Lecourieux F (2014) The basic leucine zipper transcription factor ABSCISIC ACID RESPONSE ELEMENT-BINDING FACTOR2 is an important transcriptional regulator of abscisic acid-dependent grape berry ripening processes. Plant Physiol 164(1):365–383
Medina-Puche L, Cumplido-Laso G, Amil-Ruiz F, Hoffmann T, Ring L, Rodríguez-Franco A, Caballero JL, Schwab W, Muñoz-Blanco J, Blanco-Portales R (2013) MYB10 plays a major role in the regulation of flavonoid/phenylpropanoid metabolism during ripening of Fragaria × ananassa fruits. J Exp Bot 64(6):1471–1483
Shen X, Zhao K, Liu L, Zhang K, Yuan H, Liao X, Wang Q, Guo X, Li F, Li T (2014) A role for PacMYBA in ABA-regulated anthocyanin biosynthesis in red-colored sweet cherry cv. Hong Deng (Prunus avium L.). Plant Cell Physiol 55(5):862–880
Weng L, Zhao F, Li R, Xu C, Chen K, Xiao H (2015) The zinc finger transcription factor SlZFP2 negatively regulates abscisic acid biosynthesis and fruit ripening in tomato. Physiol Plant 167(3):931–949
Larkindale J, Knight MR (2002) Protection against heat stress-induced oxidative damage in arabidopsis involves calcium, abscisic acid, ethylene, and salicylic acid. Plant Ecophysiol 128:682–713
McAtee P, Karim S, Schaffer R, David K (2013) A dynamic interplay between phytohormones is required for fruit development, maturation, and ripening. Front Plant Sci 4:79–85
Zur I, Dubas E, Golemiec E, Szechyńska-Hebda M, Janowiak F, Wędzony M (2008) Stress-induced changes important for effective androgenic induction in isolated microspore culture of triticale (× Triticosecale Wittm.). Plant Cell Tissue Org 94(3):319–328
Zur I, Dubas E, Golemiec E, Szechyńska-Hebda M, Golebiowska G, Wedzony M (2009) Stress-related variation in antioxidative enzymes activity and cell metabolism efficiency associated with embryogenesis induction in isolated microspore culture of triticale (× Triticosecale Wittm.). Plant Cell Rep 28(8):1279–1287
Van Bergen S, Kottenhagen MJ, Der Van, Meulen RM, Wang M (1999) The role of abscisic acid in induction of androgenesis: a comparative study between Hordeum vulgare L. cvs. Igri and Digger. J Plant Growth Regul 18(3):135–143
Zur I, Krzewska M, Dubas E, Gołębiowska-Pikania G, Janowiak F, Stojałowski S (2012) Molecular mapping of loci associated with abscisic acid accumulation in triticale (× Triticosecale Wittm.) anthers in response to low temperature stress inducing androgenic development. Plant Growth Regul 68(3):483–492
Dubas E, Janowiak F, Krzewska M, Hura T, Zur I (2013) Endogenous ABA concentration and cytoplasmic membrane fluidity in microspores of oilseed rape (Brassica napus L.) genotypes differing in responsiveness to androgenesis induction. Plant Cell Rep 32(9):1465–1475
Trivellini A, Ferrante A, Vernieri P, Serra G (2011) Effects of abscisic acid on ethylene biosynthesis and perception in Hibiscus rosa-sinensis L. flower development. J Exp Bot 62(15):5437–5452
Hao S, Ariizumi T, Ezura H (2017) SEXUAL STERILITY is essential for both male and female gametogenesis in tomato. Plant Cell Physiol 58(1):22–34
Xu J, Driedonks N, Rutten MJM, Vriezen WH, de Boer GJ, Rieu I (2017) Mapping quantitative trait loci for heat tolerance of reproductive traits in tomato (Solanum lycopersicum). Mol Breed 37(5):58–66
Brukhin V, Hernould M, Gonzalez N, Chevalier C, Mouras A (2003) Flower development schedule in tomato Lycopersicon esculentum cv. sweet cherry. Sex Plant Reprod 15(6):311–320
Polle E, Konzak CF, Kittrick JA (1978) Visual detection of aluminum tolerance levels in wheat by hematoxylin staining of seedling roots. Crop Sci 18(5):823–827
Alexander MP (1969) Differential staining of aborted and non-aborted Pollen. Biotech Histochem 44(3):117–122
Boavida LC, McCormick S (2007) Temperature as a determinant factor for increased and reproducible in vitro pollen germination in Arabidopsis thaliana. Plant J 52:570–582
Hendelman A, Buxdorf K, Stav R, Kravchik M, Arazi T (2012) Inhibition of lamina outgrowth following Solanum lycopersicum AUXIN RESPONSE FACTOR 10 (SlARF10) derepression. Plant Mol Biol 78(6):561–576
Hord CLH, Chen CB, Young DBJ, Clark SE, Ma H (2006) The BAM1/BAM2 receptor-like kinases are important regulators of arabidopsis early anther development. Plant Cell 18(7):1667–1680
Kim JE, Lee BW, Kim SM, Lee BM, Lee JH, Jo SH (2013) Genome-wide SNP database for marker-assisted background selection in Tomato. Korean J Breed Sci 45(3):232–239
Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L (2012) Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 7(3):562–578
Mandaokar A, Browse J (2009) MYB108 acts together with MYB24 to regulate jasmonate-mediated stamen maturation in arabidopsis. Physiol Plant 149(2):851–862
Chen CY, Cheung AY, Wu HM (2003) Actin-depolymerizing factor mediates Rac/Rop GTPase-regulated pollen tube growth. Plant Cell 15(1):237–249
Vidali L, Hepler PK (2001) Actin and pollen tube growth. Protoplasma 215(1–4):64–76
Vidali L, McKenna ST, Hepler PK (2001) Actin polymerization is essential for pollen tube growth. Mol Biol Cell 12(8):2534–2545
Su YH, Su YX, Liu YG, Zhang XS (2013) Abscisic acid is required for somatic embryo initiation through mediating spatial auxin response in Arabidopsis. Plant Growth Regul 69(2):167–176
Chen KY, Tanksley SD (2004) High-resolution mapping and functional analysis of se2.1. Genetics 168(3):1563–1573
Sapir G, Baras Z, Azmon G, Goldway M, Shafir S, Allouche A, Stern E, Stern RA (2017) Synergistic effects between bumblebees and honey bees in apple orchards increase cross pollination, seed number and fruit size. Sci Hortic 219:107–117
Sato S, Kamiyama M, Iwata T, Makita N, Furukawa H, Ikeda H (2006) Moderate increase of mean daily temperature adversely affects fruit set of Lycopersicon esculentum by disrupting specific physiological processes in male reproductive development. Ann Bot 97(5):731–738
Akhtar S, Ansary SH, Dutta AK, Karak C, Hazra P (2012) Crucial reproductive characters as screening indices for tomato (Solanum lycopersicum) under high temperature stress. J Crop Weed 8:114–117
Bhattarai U, Sharma A, Das R, Talukdar P (2016) Genetic analysis of yield and yield-attributing traits for high temperature resistance in tomato. Int J Veg Sci 22(6):585–597
Firon N, Shaked R, Peet MM, Pharr DM, Zamski E, Rosenfeld K, Althan L, Pressman E (2006) Pollen grains of heat tolerant tomato cultivars retain higher carbohydrate concentration under heat stress conditions. Sci Hortic 109(3):212–217
Pressman E, Peet MM, Pharr DM (2002) The effect of heat stress on tomato pollen characteristics is associated with changes in carbohydrate concentration in the developing anthers. Ann Bot 90(5):631–636
Ma Y, Szostkiewicz I, Korte A, Moes D, Yang Y, Christmann A, Grill E (2009) Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science 324(5930):1064–1068
Park SY, Fung P, Nishimura N, Jensen DR, Fujii H, Zhao Y, Lumba S, Santiago J, Rodrigues A, Chow TF, Alfred SE, Bonetta D, Finkelstein R, Provart NJ, Desveaux D, Rodriguez PL, McCourt P, Zhu JK, Schroeder JI, Volkman BF, Cutler SR (2009) Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science 324(5930):1068–1071
Park SY, Fung P, Nishimura N, Jensen DR, Fujii H, Zhao Y, Lumba S, Santiago J, Rodrigues A, Chow TF, Alfred SE, Bonetta D, Finkelstein R, Provart NJ, Desveaux D, Rodriguez PL, McCourt P, Zhu JK, Schroeder JI, Volkman BF, Cutler SR (2009) Abscisic acid inhibits PP2Cs via the PYR/PYL family of ABA-binding START proteins. Science 324(5930):1068–1071
Soon FF, Ng LM, Zhou XE, West GM, Kovach A, Tan MH, Suino-Powell KM, He Y, Xu Y, Chalmers MJ, Brunzelle JS, Zhang H, Yang H, Jiang H, Li J, Yong EL, Cutler S, Zhu JK, Griffin PR, Melcher K, Xu HE (2012) Molecular mimicry regulates ABA signaling by SnRK2 kinases and PP2C phosphatases. Science 335(6064):85–88
Antoni R, Gonzalez-Guzman M, Rodriguez L, Rodrigues A, Pizzio GA, Rodriguez PL (2012) Selective inhibition of clade A phosphatases type 2C by PYR/PYL/RCAR abscisic acid receptors1. Physiol Plant 158(2):970–980
Geiger D, Scherzer S, Mumm P, Marten I, Ache P, Matschi S, Liese A, Wellmann C, Al-Rasheid KAS, Grili E, Romeis T, Hedrich R (2010) Guard cell anion channel SLAC1 is regulated by CDPK protein kinases with distinct Ca2+ affinities. Proc Natl Acad Sci 107(17):8023–8028
Miao Y, Lv D, Wang P, Wang XC, Chen J, Miao C, Song CP (2006) An arabidopsis glutathione peroxidase functions as both a redox transducer and a scavenger in abscisic acid and drought stress responses. Plant Cell 18(10):2749–2766
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This work was financially supported by grants from the ISF-NSFC Joint Scientific Research Program (Grant number 31661143046) and the National Natural Science Foundation of China (Grant numbers 31572095, 31772270).
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Dai, S., Kai, W., Liang, B. et al. The functional analysis of SlNCED1 in tomato pollen development. Cell. Mol. Life Sci. 75, 3457–3472 (2018). https://doi.org/10.1007/s00018-018-2809-9
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DOI: https://doi.org/10.1007/s00018-018-2809-9