Abstract
Since the discovery of somatic embryogenesis (SE), it has been evident that nitrogen (N) metabolism is essential during morphogenesis and cell differentiation. Usually, N is supplied to cultures in vitro in three forms, ammonium (NH4+), nitrate (NO3−), and amino N from amino acids (AAs). Although most plants prefer NO3− to NH4+, NH4+ is the primary form route to be assimilated. The balance of NO3− and NH4+ determines if the morphological differentiation process will produce embryos. That the N reduction of NO3− is needed for both embryo initiation and maturation is well-established in several models, such as carrot, tobacco, and rose. It is clear that N is indispensable for SE, but the mechanism that triggers the signal for embryo formation remains unknown. Here, we discuss recent studies that suggest an optimal endogenous concentration of auxin and cytokinin is closely related to N supply to plant tissue. From a molecular and biochemical perspective, we explain N’s role in embryo formation, hypothesizing possible mechanisms that allow cellular differentiation by changing the nitrogen source.
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References
Almeida AM, Parreira JR, Santos R, Duque AS, Francisco R, Tomé DFA, Ricardo CP, Coelho AV, Fevereiro P (2012) A proteomics study of the induction of somatic embryogenesis in Medicago truncatula using 2DE and MALDI-TOF/TOF. Physiol Plant 146(2):236–249. https://doi.org/10.1111/j.1399-3054.2012.01633.x
Ara H, Jaiswal U, Jaiswal V (2000) Somatic embryogenesis and plantlet regeneration in Amrapali and Chausa cultivars of mango (Mangifera indica L.). Curr Sci 78(2):164–169
Arslan H, Güleryüz G (2005) A study on nitrate reductase activity (NRA) of geophytes from Mediterranean environment. Flora –morphol Distrib Funct Ecol Plants 200(5):434–443. https://doi.org/10.1016/j.flora.2005.02.003
Avila C, Suárez MF, Gómez-Maldonado J, Cánovas FM (2001) Spatial and temporal expression of two cytosolic glutamine synthetase genes in Scots pine: functional implications on nitrogen metabolism during early stages of conifer development. Plant J 25(1):93–102. https://doi.org/10.1111/j.1365-313X.2001.00938.x
Ávila-Sáez C, Muñoz-Chapuli R, Plomion C, Frigerio JM, Cánovas FM (2000) Two genes encoding distinct cytosolic glutamine synthetases are closely linked in the pine genome. FEBS Lett 477(3):237–243. https://doi.org/10.1016/S0014-5793(00)01796-8
Avilez-Montalvo RN, Loyola-Vargas VM (2018) Appendix A: the components of the culture media. In: Loyola-Vargas VM, Ochoa-Alejo N (eds) Plant cell culture protocols. Springer, New York, pp 493–502. https://doi.org/10.1007/978-1-4939-8594-4
Balotf S, Kavoosi G, Kholdebarin B (2016) Nitrate reductase, nitrite reductase, glutamine synthetase, and glutamate synthase expression and activity in response to different nitrogen sources in nitrogen-starved wheat seedlings. Biotechnol Appl Biochem 63(2):220–229. https://doi.org/10.1002/bab.1362
Barbier-Brygoo H, De Angeli A, Filleur S, Frachisse JM, Gambale F, Thomine S, Wege S (2011) Anion channels/transporters in plants: from molecular bases to regulatory networks. Annu Rev Plant Biol 62(1):25–51. https://doi.org/10.1146/annurev-arplant-042110-103741
Barrett JD, Park YS, Bonga JM (1997) The effectiveness of various nitrogen sources in white spruce [Picea glauca (Moench) Voss] somatic embryogenesis. Plant Cell Rep 16(6):411–415. https://doi.org/10.1007/BF01146784
Bozhkov PV, Mikhlina SB, Shiryaeva GA, Lebedenko LA (1993) Influence of nitrogen balance of culture medium on norway spruce [Picea abies (L.) Karst] somatic polyembryogenesis: high frequency establishment of embryonal-suspensor mass lines from mature zygotic embryos. J Plant Physiol 142(6):735–741. https://doi.org/10.1016/S0176-1617(11)80911-9
Brewitz E, Larsson CM, Larsson M (1995) Influence of nitrate supply on concentrations and translocation of abscisic acid in barley (Hordeum vulgare). Physiol Plant 95(4):499–506. https://doi.org/10.1111/j.1399-3054.1995.tb05515.x
Britto DT, Kronzucker HJ (2002) NH4+ toxicity in higher plants: a critical review. J Plant Physiol 159(6):567–584. https://doi.org/10.1078/0176-1617-0774
Caba JM, Centeno ML, Fernández B, Gresshoff PM, Ligero F (2000) Inoculation and nitrate alter phytohormone levels in soybean roots: differences between a supernodulating mutant and the wild type. Planta 211(1):98–104. https://doi.org/10.1007/s004250000265
Campbell WH (2001) Structure and function of eukaryotic NAD(P)H:nitrate reductase. Cell Mol Life Sci 58(2):194–204. https://doi.org/10.1007/PL00000847
Campbell RA, Durzan DJ (1975) Induction of multiple buds and needles in tissue cultures of Picea glauca. Can J Bot 53(16):1652–1657. https://doi.org/10.1139/b75-196
Cañas RA, Yesbergenova-Cuny Z, Belanger L, Rouster J, Brulé L, Gilard F, Quilleré I, Sallaud C, Hirel B (2020) NADH-GOGAT overexpression does not improve maize (Zea mays) performance even when pyramiding with NAD-IDH. GDH and GS Plants 9(2):130. https://doi.org/10.3390/plants9020130
Cantón FR, Suárez MF, Josè-Estanyol M, Cánovas FM (1999) Expression analysis of a cytosolic glutamine synthetase gene in cotyledons of Scots pine seedlings: developmental, light regulation and spatial distribution of specific transcripts. Plant Mol Biol 40(4):623–634. https://doi.org/10.1023/A:1006219205062
Carlsson J, Svennerstam H, Moritz T, Egertsdotter U, Ganeteg U (2017) Nitrogen uptake and assimilation in proliferating embryogenic cultures of Norway spruce-Investigating the specific role of glutamine. PLoS ONE 12(8):e0181785. https://doi.org/10.1371/journal.pone.0181785
Carlsson J, Egertsdotter U, Ganeteg U, Svennerstam H (2019) Nitrogen utilization during germination of somatic embryos of Norway spruce: revealing the importance of supplied glutamine for nitrogen metabolism. Trees 33(2):383–394. https://doi.org/10.1007/s00468-018-1784-y
Chamizo-Ampudia A, Sanz-Luque E, Llamas T, Ocaña-Calahorro F, Mariscal V, Carreras A, Barroso JB, Galvín A, Fernández E (2016) A dual system formed by the ARC and NR molybdoenzymes mediates nitrite-dependent NO production in Chlamydomonas. Plant Cell Envirom 39(10):2097–2107. https://doi.org/10.1111/pce.12739
Chapin FS, Walter CHS, Clarkson DT (1988) Growth response of barley and tomato to nitrogen stress and its control by abscisic acid, water relations and photosynthesis. Planta 173(3):352–366. https://doi.org/10.1007/BF00401022
Chen B, Fiers M, Dekkers BJ, Maas L, van Esse GW, Angenent GC, Zhao Y, Boutilier K (2021) ABA signalling promotes cell totipotency in the shoot apex of germinating embryos. J Exp Bot 72(18):6418–6436. https://doi.org/10.1093/jxb/erab306
Corey KA, Barker AV, Craker LE (1987) Ethylene evolution by tomato plants under stress of ammonium toxicity. HortScience 22(3):471–473
Cunha A, Fernandes-Ferreira M (1999) Influence of medium parameters on somatic embryogenesis from hypocotyl explants of flax (Linum usitatissimum L.). J Plant Physiol 155(4):591–597. https://doi.org/10.1016/S0176-1617(99)80059-5
Dahrendorf J, Clapham D, Egertsdotter U (2018) Analysis of nitrogen utilization capability during the proliferation and maturation phases of Norway spruce (Picea abies (L.) H Karst.) somatic embryogenesis. Forests 9(6):288. https://doi.org/10.3390/f9060288
Dal Vesco LL, Guerra MP (2001) The effectiveness of nitrogen sources in Feijoa somatic embryogenesis. Plant Cell Tissue Organ Cult 64(1):19–25. https://doi.org/10.1023/A:1010635926146
De Angeli A, Monachello D, Ephritikhine G, Frachisse JM, Thomine S, Gambale F, Barbier-Brygoo H (2006) The nitrate/proton antiporter AtClCa mediates nitrate accumulation in plant vacuoles. Nature 442(7105):939–942. https://doi.org/10.1038/nature05013
de la Torre F, García-Gutiérrez A, Crespillo R, Cantón FR, Ávila C, Cánovas FM (2002) Functional expression of two pine glutamine synthetase genes in bacteria reveals that they encode cytosolic holoenzymes with different molecular and catalytic properties. Plant Cell Physiol 43(7):802–809. https://doi.org/10.1093/pcp/pcf094
de la Torre F, Cañas RA, Pascual MB, Avila C, Cánovas FM (2014) Plastidic aspartate aminotransferases and the biosynthesis of essential amino acids in plants. J Exp Bot 65(19):5527–5534. https://doi.org/10.1093/jxb/eru240
Dhir SK, Yadava UL (1995) Somatic embryogenesis using immature zygotic embryos from developing fruits of papaya (Carica papaya). HortScience 30(4):783. https://doi.org/10.21273/HORTSCI.30.4.783E
Dodeman VL, Ducreux G (1996) Isozyme patterns in zygotic and somatic embryogenesis of carrot. Plant Cell Rep 16(1/2):101–105. https://doi.org/10.1007/BF01275460
Domzalska L, Kedracka-Krok S, Jankowska U, Grzyb M, Sobczak M, Rybczynski JJ, Mikula A (2017) Proteomic analysis of stipe explants reveals differentially expressed proteins involved in early direct somatic embryogenesis of the tree fern Cyathea delgadii Sternb. Plant Sci. https://doi.org/10.1016/j.plantsci.2017.01.017
Dos Santos MF, Memelink J, Offringa R (2009) Auxin-induced, SCFTIR1-mediated poly-ubiquitination marks AUX/IAA proteins for degradation. Plant J 59(1):100–109. https://doi.org/10.1111/j.1365-313X.2009.03854.x
Dougall DK (1980) Nutrition and metabolism. In: Staba EJ (ed) Plant tissue culture as a source of biochemicals. CRC Press Inc., Boca Raton, pp 21–58
Dougall DK, Verma DC (1978) Growth and embryo formation in wild carrot suspension cultures with ammonium ion as a sole nitrogen source. In Vitro Cell Dev Biol -Plant 14(2):180–182. https://doi.org/10.1007/BF02618220
Durzan DJ (1988) Applications of cell and tissue culture in tree improvement. In: Bock G, Marsh J (eds) Applications of plant cell and tissue culture. Wiley, Chichester, pp 36–58
Dziewit K, Pêncík A, Dobrzyńska K, Novák O, Szal B, Podgórska A (2021) Spatiotemporal auxin distribution in Arabidopsis tissues is regulated by anabolic and catabolic reactions under long-term ammonium stress. BMC Plant Biol 21(1):602. https://doi.org/10.1186/s12870-021-03385-9
Elkonin LA, Pakhomova NV (2000) Influence of nitrogen and phosphorus on induction embryogenic callus of sorghum. Plant Cell Tissue Organ Cult 61(2):115–123. https://doi.org/10.1023/A:1006472418218
Endres L, Souza BM, Mercier H (2002) In vitro nitrogen nutrition and hormonal pattern in bromeliads. In Vitro Cell Dev Biol -Plant 38(5):481–486. https://doi.org/10.1079/IVP2002323
Eui CY, Soh WY (1997) Effect of ammonium ion on morphogenesis from cultured cotyledon explants of Panax ginseng. J Plant Biol 40(1):21–26. https://doi.org/10.1007/BF03030316
Fei H, Vessey JK (2003) Involvement of cytokininin the stimulationof nodulation by low concentration of ammonium in Pisum sativum. Physiol Plant 118(3):447–455. https://doi.org/10.1034/j.1399-3054.2003.00123.x
Fletcher JS (1982) Control of nitrogen assimilation in suspension cultures of Paul’s scarlet rose. In: Fujiwara A (ed) Plant tissue culture 1982. The Japanese Association for Plant Tissue Culture, pp 229–230
Fontaine JX, Tercé-Laforgue T, Armengaud P, Clément G, Renou JP, Pelletier S, Catterou M, Azzopardi M, Gibon Y, Lea PJ, Hirel B, Dubois F (2012) Characterization of a NADH-dependent glutamate dehydrogenase mutant of Arabidopsis demonstrates the key role of this enzyme in root carbon and nitrogen metabolism. Plant Cell 24(10):4044–4065. https://doi.org/10.1105/tpc.112.103689
Franklin CI, Dixon RA (2003) Callus and cell suspension cultures. In: Dixon RA, Gonzales RA (eds) Plant cell culture: a practical approach. Oxford University Press, Oxford, pp 1–26
Fuentes-Cerda CFJ, Monforte-González M, Méndez-Zeel M, Rojas-Herrera R, Loyola-Vargas VM (2001) Modification of the embryogenic response of Coffea arabica by nitrogen source. Biotechnol Lett 23(6):1341–1343. https://doi.org/10.1023/A:1010545818671
Gamborg OL (1970) The effects of amino acids and ammonium on the growth of plant cells in suspension culture. Plant Physiol 45(4):372–375. https://doi.org/10.1104/pp.45.4.372
Gamborg OL (1984) Plant cell cultures: nutrition and media. In: Vasil IK (ed) Cell culture and somatic cell genetics of plants vol. 1. laboratory procedures and their applications. Academic Press Inc., Orlando, pp 18–26
Gamborg OL, Shyluk JP (1970) The culture of plant cells with ammonium salts as the sole nitrogen source. Plant Physiol 45(5):598–600. https://doi.org/10.1104/pp.45.5.598
Garnica M, Houdusse F, Zamarreño AM, Garcia-Mina JM (2010) The signal effect of nitrate supply enhances active forms of cytokinins and indole acetic content and reduces abscisic acid in wheat plants grown with ammonium. J Plant Physiol 167(15):1264–1272. https://doi.org/10.1016/j.jplph.2010.04.013
George EF, De Klerk G-J (2008) The components of plant tissue culture media I: macro and micro nutrients. In: George EF, Hall MA, De Klerk GJ (eds) Plant propagation by tissue culture. Springer, Dordrecht, pp 65–102. https://doi.org/10.1007/978-1-4020-5005-3_3
George EF, Hall MA, De Klerk G-J (2008) The components of plant tissue culture media II: organic additions, osmotic and pH effects, and support systems. In: George EF, Hall MA, De Klerk GJ (eds) Plant propagation by tissue culture. Springer, Dordrecht, pp 115–173. https://doi.org/10.1007/978-1-4020-5005-3_4
Gleddie S, Keller W, Setterfield G (1982) In vitro morphogenesis from tissues, cells, and protoplasts of Solanum melongena L. In: Fujiwara A (ed) Plant tissue culture 1982. The Japanese Association for Plant Tissue Culture, pp 139–140
González-Benito ME, Frota-Chagas Carballo JM, Pérez C (1997) Somatic embryogenesis of an early cotton cultivar. Pesqui Agropecu Bras 32:485–488
Guevin TG, Kirby EG (1997) Induction of embryogenesis in cultured mature zygotic embryos of Abies fraseri (Pursh) Poir. Plant Cell Tissue Organ Cult 49(3):219–222. https://doi.org/10.1023/A:1005747026269
Gutierrez E, Gallego P, Alonso A, Blazquez A, Martin L, Fernandez J, Dominguez L, Rioja C, Guerra H, Villalobos N (2010) Nitrogen compounds in embryogenic and non-embryogenic calluses of Medicago arborea L. In Vitro Cell Dev Biol-Plant 46(3):257–264. https://doi.org/10.1007/s11627-009-9273-z
Habib D, Zia M, Bibi Y, Abbasi BH, Chaudhary MF (2015) Response of nitrogen assimilating enzymes during in vitro culture of Agyrolobium roseum. Biologia 70(4):478–485. https://doi.org/10.1515/biolog-2015-0060
Halperin W (1969) Morphogenesis in cell cultures. Annu Rev Plant Physiol. https://doi.org/10.1146/annurev.pp.20.060169.002143
Halperin W, Wetherell DF (1965) Ammonium requirement for embryogenesis in vitro. Nature 205(4970):519–520. https://doi.org/10.1038/205519a0
Hamasaki RM, Purgatto E, Mercier H (2005) Glutamine enhances competence for organogenesis in pineapple leaves cultivated in vitro. Braz J Plant Physiol 17(4):383–389. https://doi.org/10.1590/S1677-04202005000400006
Han GY, Chi JN, Wang XF, Zhang GY, Ma ZY (2010) Cloning and characterization of a nitrite reductase gene related to somatic embryogenesis in Gossypium hirsutum. Afr J Biotechnol 9(9):1304–1311
Higashi K, Kamada H, Harada H (1996) The effects of reduced nitrogenous compounds suggests that glutamine synthetase activity is involved in the development of somatic embryos in carrot. Plant Cell Tissue Organ Cult 45(2):109–114. https://doi.org/10.1007/BF00048752
Higashi K, Shiota H, Kamada H (1998) Patterns of expression of the genes for glutamine synthetase isoforms during somatic and zygotic embryogenesis in carrot. Plant Cell Physiol 39(4):418–424. https://doi.org/10.1093/oxfordjournals.pcp.a029385
Ida S, Mikami B (1986) Spinach ferredoxin-nitrite reductase: a purification procedure and characterization of chemical properties. Biochim Biophys Acta 871(2):167–176. https://doi.org/10.1016/0167-4838(86)90170-6
Ivanova M, Van Staden J (2009) Nitrogen source, concentration, and NH4+:NO3- ratio influence shoot regeneration and hyperhydricity in tissue cultured Aloe polyphylla. Plant Cell Tissue Organ Cult 99(2):167–174. https://doi.org/10.1007/s11240-009-9589-8
Jordan DB, Fletcher JS (1980) Nitrate assimilation in suspension cultures of Paul’s scarlet rose. Can J Bot 58(9):1088–1094. https://doi.org/10.1139/b80-132
Joy RW, McIntyre DD, Vogel HJ, Thorpe TA (1996) Stage-specific nitrogen metabolism in developing carrot somatic embryos. Physiol Plant 97(1):149–159. https://doi.org/10.1111/j.1399-3054.1996.tb00491.x
Joy RW, Vogel HJ, Thorpe TA (1997) Inorganic nitrogen metabolism in embryogenic white spruce cultures: a nitrogen 14/15 NMR study. J Plant Physiol 151(3):306–315. https://doi.org/10.1016/S0176-1617(97)80257-X
Kamada H, Harada H (1982) Studies on nitrogen metabolism during somatic embryogenesis in carrot. In: Fujiwara A (ed) Plant tissue culture 1982. The Japanese Association for Plant Tissue Culture, Tokyo, pp 115–116
Kamada H, Harada H (1984a) Changes in endogenous amino acid compositions during somatic embryogenesis in Daucus carota L. Plant Cell Physiol 25(1):27–38. https://doi.org/10.1093/oxfordjournals.pcp.a076693
Kamada H, Harada H (1984b) Studies on nitrogen metabolism during somatic embryogenesis in carrot. I. Utilization of α-alanine as a nitrogen source. Plant Sci Lett 33(1):7–13. https://doi.org/10.1016/0304-4211(84)90062-2
Kamada-Nobusada T, Makita N, Kojima M, Sakakibara H (2013) Nitrogen-dependent regulation of de novo cytokinin biosynthesis in rice: the role of glutamine metabolism as an additional signal. Plant Cell Physiol 54(11):1881–1893. https://doi.org/10.1093/pcp/pct127
Khlin S, Tremblay FM (1995) Maturation of black spruce somatic embryos. Part I. Effect of L-glutamine on the number and germinability of somatic embryos. Pant Cell Tissue Organ Cult 41(1):23–32
Kiba T, Krapp A (2016) Plant nitrogen acquisition under low availability: Regulation of uptake and root architecture. Plant Cell Physiol 57(4):707–714. https://doi.org/10.1093/pcp/pcw052
Kiba T, Kudo T, Kojima M, Sakakibara H (2011) Hormonal control of nitrogen acquisition: roles of auxin, abscisic acid, and cytokinin. J Exp Bot 62(4):1399–1409. https://doi.org/10.1093/jxb/erq410
Kirby EG (1982) The effects of organic nitrogen sources on growth of cell cultures of Douglas-fir. Physiol Plant 56(1):114–117. https://doi.org/10.1111/j.1399-3054.1982.tb04908.x
Kishorekumar R, Bulle M, Wany A, Gupta KJ (2020) An overview of important enzymes involved in nitrogen assimilation of plants. In: Gupta KJ (ed) Nitrogen metabolism in plants: methods and protocols. Springer, New York, pp 1–13. https://doi.org/10.1007/978-1-4939-9790-9_1
Konishi N, Saito M, Imagawa F, Kanno K, Yamaya T, Kojima S (2018) Cytosolic glutamine synthetase isozymes play redundant roles in ammonium assimilation under low-ammonium conditions in roots of Arabidopsis thaliana. Plant Cell Physiol 59(3):601–613. https://doi.org/10.1093/pcp/pcy014
Kormuťák A, Vooková B (1997) Biochemical variation between non-embryogenic and embryogenic calli of silver fir. Biol Plant 39(1):125–130. https://doi.org/10.1023/A:1000325510211
Kouadio Oi Kouadio S, Yapo Edwige SS, Kouassi Kan M, Silue O, Koffi E, Kouakou Tanoh H (2017) Improved callogenesis and somatic embryogenesis using amino acids and plant growth regulators combination in pineapple [Ananas comosus (L.) merr .(Bromeliaceae)]. Eur J Biotechnol Biosc 5(5):6–16
Krapp A (2015) Plant nitrogen assimilation and its regulation: a complex puzzle with missing pieces. Curr Opin Plant Biol. https://doi.org/10.1016/j.pbi.2015.05.010
Kronenberger J, Lepingle A, Caboche M, Vaucheret H (1993) Cloning and expression of distinct nitrite reductases in tobacco leaves and roots. Mol Gen Genet 236(2/3):203–208. https://doi.org/10.1007/BF00277113
Krouk G, Lacombe B, Bielach A, Perrine-Walker F, Malinska K, Mounier E, Hoyerova K, Tillard P, Leon S, Ljung K, Zazimalová E, Benková E, Nacry P, Gojon A (2010) Nitrate-regulated auxin transport by NRT1.1 defines a mechanism for nutrient sensing in plants. Dev Cell 18(6):927–937. https://doi.org/10.1016/j.devcel.2010.05.008
Kudoyarova GR, Farkhutdinov RG, Veselov SYu (1997) Comparison of the effects of nitrate and ammonium forms of nitrogen on auxin content in roots and the growth of plants under different temperature conditions. Plant Growth Regul 23(3):207–208. https://doi.org/10.1023/A:1005990725068
Kwinta J, Bielawski W (1998) Glutamate dehydrogenase in higher plants. Acta Physiol Plant 20(4):453–463. https://doi.org/10.1007/s11738-998-0033-1
LaCuesta M, Saiz-Fernández I, Podlesáková K, Miranda-Apodaca J, Novák O, Dolezal K, De Diego N (2018) The trans and cis zeatin isomers play different roles in regulating growth inhibition induced by high nitrate concentrations in maize. Plant Growth Regul 85(2):199–209. https://doi.org/10.1007/s10725-018-0383-7
Lai F-M, Senaratna T, McKersie BD (1992) Glutamine enhances storage protein synthesis in Medicago sativa L. somatic embryos. Plant Sci 87(1):69–77. https://doi.org/10.1016/0168-9452(92)90194-Q
Lam HM, Coschigano KT, Oliveira IC, Melo-Oliveira R, Coruzzi GM (1996) The molecular-genetics of nitrogen assimilation into amino acids in higher plants. Annu Rev Plant Physiol Plant Mol Biol. https://doi.org/10.1146/annurev.arplant.47.1.569
Lasa B, Frechilla S, paricio-Tejo PM, Lamsfus C, (2002) Role of glutamate dehydrogenase and phosphoenolpyruvate carboxylase activity in ammonium nutrition tolerance in roots. Plant Physiol Biochem 40(11):969–976. https://doi.org/10.1016/S0981-9428(02)01451-1
Lea PJ, Ireland RJ (1999) Nitrogen metabolism in higher plants. In: Singh BK (ed) Plant amino acids: biochemistry and biotechnology. CRC Press, Boca Raton, pp 1–47
Lee HJ, Abdula SE, Jang DW, Park SH, Yoon UH, Jung YJ, Kang KK, Nou IS, Cho YG (2013) Overexpression of the glutamine synthetase gene modulates oxidative stress response in rice after exposure to cadmium stress. Plant Cell Rep 32(10):1521–1529. https://doi.org/10.1007/s00299-013-1464-8
Leljak D, Jelaska S (1995) Callus formation and somatic embryo production in pumpkin Cucurbita pepo L. explants on hormone free medium. Period Biol 97(4):327–332
Leljak-Levanic D, Bauer N, Mihaljevic S, Jelaska S (2004a) Changes in DNA methylation during somatic embryogenesis in Cucurbita pepo L. Plant Cell Rep 23(3):120–127. https://doi.org/10.1007/s00299-004-0819-6
Leljak-Levanic D, Bauer N, Mihaljevic S, Jelaska S (2004b) Somatic embryogenesis in pumpkin (Cucurbita pepo L.): control of somatic embryo development by nitrogen compounds. J Plant Physiol 161(2):229–236. https://doi.org/10.1078/0176-1617-01055
Léran S, Varala K, Boyer JC, Chiurazzi M, Crawford N, Daniel-Vedele F, David L, Dickstein R, Fernandez E, Forde B, Gassmann W, Geiger D, Gojon A, Gong JM, Halkier BA, Harris JM, Hedrich R, Limami AM, Rentsch D, Seo M, Tsay YF, Zhang M, Coruzzi G, Lacombe B (2014) A unified nomenclature of NITRATE TRANSPORTER 1/PEPTIDE TRANSPORTER family members in plants. Trends Plant Sci 19(1):5–9. https://doi.org/10.1016/j.tplants.2013.08.008
Lima JE, Kojima S, Takahashi H, Von Wirén N (2010) Ammonium triggers lateral root branching in Arabidopsis in an AMMONIUM TRANSPORTER1;3-dependent manner. Plant Cell 22(11):3621–3633. https://doi.org/10.1105/tpc.110.076216
Linkohr BI, Williamson LC, Fitter AH, Ottoline Leyser HM (2002) Nitrate and phosphate availability and distribution have different effects on root system architecture of Arabidopsis. Plant J 29(6):751–760. https://doi.org/10.1046/j.1365-313X.2002.01251.x
Llebrés MT, Avila C, Cánovas FM, Klimaszewska K (2018) Root growth of somatic plants of hybrid Pinus strobus (L.) and P. wallichiana (A. B. Jacks.) is affected by the nitrogen composition of the somatic embryo germination medium. Trees 32(2):371–381. https://doi.org/10.1007/s00468-017-1635-2
Loulakakis KA, Roubelakis-Angelakis KA (1991) Plant NAD(H)-glutamate dehydrogenase consists of two subunit polypeptides and their participation in the seven isoenzymes occurs in an ordered ratio. Plant Physiol 97(1):104–111. https://doi.org/10.1104/pp.97.1.104
Loulakakis KA, Roubelakis-Angelakis KA (1992) Ammonium-induced increase in NADH-glutamate dehydrogenase activity is caused by de-novo synthesis of the a-subunit. Planta 187(3):322–327. https://doi.org/10.1007/BF00195655
Loyola-Vargas VM, Ochoa-Alejo N (2016) Somatic embryogenesis. An overview. In: Loyola-Vargas VM, Ochoa-Alejo N (eds) Somatic embryogenesis. Fundamental aspects and applications. Springer, pp 1–10. https://doi.org/10.1007/978-3-319-33705-0_1
Loyola-Vargas VM, De-la-Peña C, Galaz-Ávalos RM, Quiroz-Figueroa FR (2008) Plant tissue culture. In: Walker JM, Rapley R (eds) Molecular biomethods handbook. Humana Press, Totowa, pp 875–904. https://doi.org/10.1007/978-1-60327-375-6_50
Loyola-Vargas VM, Avilez-Montalvo JR, Avilez-Montalvo RN, Márquez-López RE, Galaz-Ávalos RM, Mellado-Mojica E (2016) Somatic embryogenesis in Coffea spp. In: Loyola-Vargas VM, Ochoa-Alejo N (eds) Somatic embryogenesis. Fundamental aspects and applications. Springer, pp 241–266. https://doi.org/10.1007/978-3-319-33705-0_15
McDonald TR, Ward JM (2016) Evolution of electrogenic ammonium transporters (AMTs). Front Plant Sci. https://doi.org/10.3389/fpls.2016.00352
Menke-Milczarek I, Zimny J (2001) NH4+ and NO3- requirement for wheat somatic embryogenesis. Acta Physiol Plant 23(1):37–42. https://doi.org/10.1007/s11738-001-0020-2
Meyer C, Stitt M (2001) Nitrate reduction and signalling. In: Lea PJ, Morot-Gaudry JF (eds) Plant nitrogen. Springer, Berlin, pp 37–59. https://doi.org/10.1007/978-3-662-04064-5_2
Miflin BJ, Habash DZ (2002) The role of glutamine synthetase and glutamate dehydrogenase in nitrogen assimilation and possibilities for improvement in the nitrogen utilization of crops. J Exp Bot 53(370):979–987. https://doi.org/10.1093/jexbot/53.370.979
Miflin BJ, Lea PJ (1982) Ammonia assimilation and amino acid metabolism. In: Boulter D, Parthier B (eds) Nucleic acids and proteins in plants I. Structure, biochemistry and physiology of proteins. Springer, Berlin, pp 5–64. https://doi.org/10.1007/978-3-642-68237-7_2
Mihaljevic S, Radic S, Bauer N, Garic R, Mihaljevic B, Horvat G, Leljak-Levanic D, Jelaska S (2011) Ammonium-related metabolic changes affect somatic embryogenesis in pumpkin (Cucurbita pepo L.). J Plant Physiol 168(16):1943–1951. https://doi.org/10.1016/j.jplph.2011.05.025
Mordhorst AP, Lörz H (1993) Embryogenesis and development of isolated barley (Hordeum vulgare L.) microspores are influenced by the amount and composition of nitrogen sources in culture media. J Plant Physiol 142(4):485–492. https://doi.org/10.1016/S0176-1617(11)81256-3
Mott RL, Cordts JM, Larson AM (1985) Nitrogen and growth regulator effects on shoot and root growth of soybean in vitro. In: Henke CM, Hughes KW, Constantin MJ, Hollaender A, Wilson CM (eds) Tissue culture in forestry and agriculture. Basic life sciences. Springer, Boston, pp 336–337. https://doi.org/10.1007/978-1-4899-0378-5_46
Murillo E, Sánchez de Jiménez E (1984) Alternative pathways for ammonium assimilation in Bouvardia ternifolia cell suspension cultures. J Plant Physiol 117(1):57–68. https://doi.org/10.1016/S0176-1617(84)80016-4
Negi J, Matsuda O, Nagasawa T, Oba Y, Takahashi H, Kawai-Yamada M, Uchimiya H, Hashimoto M, Iba K (2008) CO2 regulator SLAC1 and its homologues are essential for anion homeostasis in plant cells. Nature 452(7186):483–486. https://doi.org/10.1038/nature06720
Neumann KH (1966) Wurzelbidung und Nukleinsäuregehalt bei Phloem-Gewebekulturen der Karottenwurzel auf synthetischem Nährmedium. Cong Coll Univ Liege 38:96–102
Neumann KH, Kumar A, Imani J (2009) Plant cell and tissue culture—a tool in biotechnology. Springer, Heidelberg
Nic-Can GI, Loyola-Vargas VM (2016) The role of the auxins during somatic embryogenesis. In: Loyola-Vargas VM, Ochoa-Alejo N (eds) Somatic Embryogenesis Fundamental Aspects and Applications. Springe, r, pp 171–181. https://doi.org/10.1007/978-3-319-33705-0_10
Nowak B, Miczynski K, Hudy L (2007) The effect of total inorganic nitrogen and the balance between its ionic forms on adventitious bud formation and callus growth of “Wegierka Zwykla” plum (Prunus domestica L.). Acta Physiol Plant 29(5):479–484. https://doi.org/10.1007/s11738-007-0058-x
Ogawa T (2000) Improvement of cell culture conditions for rice. Jap Agricul Res Quart 34(4):215–224
Ogita S, Sasamoto H, Yeung EC, Thorpe TA (2001) The effects of glutamine on the maintenance of embryogenic cultures of Cryptomeria japonica. In Vitro Cell Dev Biol -Plant 37(2):268–273. https://doi.org/10.1007/s11627-001-0048-4
Olsen FL (1987) Induction of microspore embryogenesis in cultured anthers of Hordeum vulgare. The effects of ammonium, nitrate, glutamine and aspargine as nitrogen sources. Carlsberg Res Commun 52(6):393–404. https://doi.org/10.1007/BF02907527
Orsel M, Krapp A, Daniel-Vedele F (2002) Analysis of the NRT2 nitrate transporter family in Arabidopsis. Structure and gene expression. Plant Physiol 129(2):886–896. https://doi.org/10.1104/pp.005280
Palmer SJ, Berridge DM, McDonald AJS, Davies WJ (1996) Control of leaf expansion in sunflower (Helianthus annuus L.) by nitrogen nutrition. J Exp Bot 47(3):359–368. https://doi.org/10.1093/jxb/47.3.359
Pencik A, Tureková V, Paulisiç S, Rolcìk J, Strnad M, Mihaljevic S (2015) Ammonium regulates embryogenic potential in Cucurbita pepo through pH-mediated changes in endogenous auxin and abscisic acid. Plant Cell Tissue Organ Cult 122(1):89–100. https://doi.org/10.1007/s11240-015-0752-0
Pérez-Rodríguez MJP, Suárez MF, Heredia R, Ávila C, Breton D, Trontin JF, Filonova L, Bozhkov P, Von Arnold S, Harvengt L, Cánovas FM (2006) Expression patterns of two glutamine synthetase genes in zygotic and somatic pine embryos support specific roles in nitrogen metabolism during embryogenesis. New Phytol 169(1):35–44. https://doi.org/10.1111/j.1469-8137.2005.01551.x
Peuke AD, Jeschke WD, Hartung W (1998) Foliar application of nitrate or ammonium as sole nitrogen supply in Ricinus communis. II. The flows of cations, chloride and abscisic acid. New Phytol 140(4):625–636. https://doi.org/10.1046/j.1469-8137.1998.00304.x
Poitout A, Crabos A, Petrick I, Novák O, Krouk G, Lacombe B, Ruffel S (2018) Responses to systemic nitrogen signaling in Arabidopsis roots involve trans-zeatin in shoots. Plant Cell 30(6):1243–1257. https://doi.org/10.1105/tpc.18.00011
Pullman GS, Bucalo K (2014) Pine somatic embryogenesis: analyses of seed tissue and medium to improve protocol development. New for 45(3):353–377. https://doi.org/10.1007/s11056-014-9407-y
Quiroz-Figueroa FR, Rojas-Herrera R, Galaz-Ávalos RM, Loyola-Vargas VM (2006) Embryo production through somatic embryogenesis can be used to study cell differentiation in plants. Plant Cell Tissue Organ Cult 86(3):285–301. https://doi.org/10.1007/s11240-006-9139-6
Rahayu YS, Walch-Liu P, Neumann G, Römheld V, von Wirén N, Bangerth F (2005) Root-derived cytokinins as long-distance signals for NO3–induced stimulation of leaf growth. J Exp Bot 56(414):1143–1152. https://doi.org/10.1093/jxb/eri107
Raj Bhansali R (1990) Somatic embryogenesis and regeneration of in plantlets in Pomegranate. Ann Bot 66(3):249–253. https://doi.org/10.1093/oxfordjournals.aob.a088022
Ramage CM, Williams RR (2002) Mineral nutrition and plant morphogenesis. In Vitro Cell Dev Biol-Plant 38(2):116–124. https://doi.org/10.1079/IVP2001269
Raven JA (1986) Biochemical disposal of excess H+ in growing plants? New Phytol 104(2):175–206. https://doi.org/10.1111/j.1469-8137.1986.tb00644.x
Reinbothe C, Diettrich B, Luckner M (1990) Regeneration of plants from somatic embryos of Digitalis lanata. J Plant Physiol 137(2):224–228. https://doi.org/10.1016/S0176-1617(11)80085-4
Reinert J (1958) Morphogenese und ihre Kontrolle an Gewebekulturen aus Carotten. Naturwissensch. https://doi.org/10.1007/BF00640240
Reinert J, Tazawa M, Semenoff S (1967) Nitrogen compounds as factors of the embryogenesis in vitro. Nature 216(5121):1215–1216. https://doi.org/10.1038/2161215a0
Rose RJ (2019) Somatic embryogenesis in the Medicago truncatula model: cellular and molecular mechanisms. Front Plant Sci. https://doi.org/10.3389/fpls.2019.00267
Samson NP, Campa C, Gal LL, Noirot M, Thomas G, Lokeswari TS, Kochko Ad (2006) Effect of primary culture medium composition on high frequency somatic embryogenesis in different Coffea species. Plant Cell Tissue Organ Cult 86(1):37–45. https://doi.org/10.1007/s11240-006-9094-2
Sánchez de Jiménez E, Fernández L (1983) Biochemical parameters to assess cell differentiation of Bouvardia ternifolia schlecht callus. Planta 158(5):377–383. https://doi.org/10.1007/BF00397728
Schons J, Galvao BO (1999) Nitrate reductase activity (EC 1.6.6.1) in the somatic embryogenesis of carrots, Daucus carota L. Agrociencia Chile 15(1):27–32
Smith DL, Krikorian AD (1989) Release of somatic embryogenic potential from excised zygotic embryos of carrot and maintenance of proembryonic cultures in hormone-free medium. Am J Bot 76(12):1832–1843. https://doi.org/10.1002/j.1537-2197.1989.tb15172.x
Smith DL, Krikorian AD (1990) Somatic embryogenesis of carrot in hormone-free medium: external pH control over morphogenesis. Am J Bot 77(12):1634–1647. https://doi.org/10.1002/j.1537-2197.1990.tb11403.x
Smith DL, Krikorian AD (1991) Growth and maintenance of an embryogenic cell culture of daylily (Hemerocallis) on hormone-free medium. Ann Bot 67(5):443–449. https://doi.org/10.1093/oxfordjournals.aob.a088180
Smith DL, Krikorian AD (1992) Low external pH prevents cell elongation but not multiplication of embryogenic carrot cells. Physiol Plant 84(4):495–501. https://doi.org/10.1111/j.1399-3054.1992.tb04696.x
Soulen TK, Olson LC (1969) Glutamate dehydrogenase activity in soybean and the effect on it of amino acid and growth substances. Planta 86(2):205–208. https://doi.org/10.1007/BF00379830
Sreedhar L, Bewley JD (1998) Nitrogen- and sulfur-containing compounds enhance the synthesis of storage reserves in developing somatic embryos of alfalfa (Medicago sativa L.). Plant Sci 134(1):31–44. https://doi.org/10.1016/S0168-9452(98)00047-8
Su YH, Liu YB, Bai B, Zhang XS (2015) Establishment of embryonic shoot-root axis is involved in auxin and cytokinin response during Arabidopsis somatic embryogenesis. Front Plant Sci. https://doi.org/10.3389/fpls.2014.00792
Swamy NR, Ugandhar T, Praveen M, Venkataiah P, Rambabu M, Upender M, Subhash K (2005) Somatic embryogenesis and plantlet regeneration from cotyledon and leaf explants of Solanum surattense. Indian J Biotecnol 4(3):414–418
Tanaka S, Ida S, Irifune K, Oeda K, Morikawa H (1994) Nucleotide sequence of a gene for nitrite reductase from Arabidopsis thaliana. DNA Seq 5(1):57–61. https://doi.org/10.31109/10425179409039705
Tazawa M, Reinert J (1969) Extracellular and intracellular chemical environments in relation to embryogenesis in vitro. Protoplasma 68(1–2):157–173. https://doi.org/10.1007/BF01247902
Tercé-Laforgue T, Bedu M, Dargel-Grafin C, Dubois F, Gibon Y, Restivo FM, Hirel B (2013) Resolving the role of plant glutamate dehydrogenase: II. Physiological characterization of plants overexpressing the two enzyme subunits individually or simultaneously. Plant Cell Physiol 54(10):1635–1647. https://doi.org/10.1093/pcp/pct108
Tercé-Laforgue T, Clément G, Marchi L, Restivo FM, Lea PJ, Hirel B (2015) Resolving the role of plant NAD-glutamate dehydrogenase: III. Overexpressing individually or simultaneously the two enzyme subunits under salt stress induces changes in the leaf metabolic profile and increases plant biomass production. Plant Cell Physiol 56(10):1918–1929. https://doi.org/10.1093/pcp/pcv114
Tobin AK, Yamaya T (2001) Cellular compartmentation of ammonium assimilation in rice and barley. J Exp Bot 52(356):591–604. https://doi.org/10.1093/jexbot/52.356.591
Tsai CJ, Saunders JW (1999) Evaluation of sole nitrogen sources for shoot and leaf disc cultures of sugarbeet. Plant Cell Tissue Organ Cult 59(1):47–56. https://doi.org/10.1023/A:1006344514809
Uc-Chuc MÁ, Pérez-Hernández CA, Galaz-Ávalos RM, Brito-Argáez L, Aguilar-Hernández V, Loyola-Vargas VM (2020) YUCCA-mediated biosynthesis of the auxin IAA is required during the somatic embryogenic induction process in Coffea canephora. Int J Mol Sci 21(13):4751. https://doi.org/10.3390/ijms21134751
Vega A, O’Brien JA, Gutiérrez RA (2019) Nitrate and hormonal signaling crosstalk for plant growth and development. Curr Opin Plant Biol. https://doi.org/10.1016/j.pbi.2019.10.001
Vidal EA, Araus V, Lu C, Parry G, Green PJ, Coruzzi GM, Gutiérrez RA (2010) Nitrate-responsive miR393/AFB3 regulatory module controls root system architecture in Arabidopsis thaliana. Proc Natl Acad Sci (USA) 107(9):4477–4482. https://doi.org/10.1073/pnas.0909571107
Wadsworth GJ (1997) The plant aspartate aminotransferase gene family. Physiol Plant 100(4):998–1006. https://doi.org/10.1111/j.1399-3054.1997.tb00028.x
Walch-Liu P, Neumann G, Bangerth F, Engels C (2000) Rapid effects of nitrogen form on leaf morphogenesis in tobacco. J Exp Bot 51(343):227–237. https://doi.org/10.1093/jexbot/51.343.227
Walker KA, Sato SJ (1981) Morphogenesis in callus tissue of Medicago sativa: The role of ammonium ion in somatic embryogenesis. Plant Cell Tissue Organ Cult 1(1):109–121. https://doi.org/10.1007/BF02318910
Wang M, Shen Q, Xu G, Guo S (2014) New insight into the strategy for nitrogen metabolism in plant cells. In: Jeon KW (ed) international review of cell and molecular biology. Elsevier, San Diego, pp 1–37. https://doi.org/10.1016/B978-0-12-800180-6.00001-3
Wetherell DF, Dougall DK (1976) Sources of nitrogen supporting growth and embryogenesis in cultured wild carrot tissue. Physiol Plant 37(2):97–103. https://doi.org/10.1111/j.1399-3054.1976.tb03939.x
Xu J, Zha M, Li Y, Ding Y, Chen L, Ding C, Wang S (2015) The interaction between nitrogen availability and auxin, cytokinin, and strigolactone in the control of shoot branching in rice (Oryza sativa L.). Plant Cell Rep 34(9):1647–1662. https://doi.org/10.1007/s00299-015-1815-8
Yang G, Wei Q, Huang H, Xia J (2020) Amino acid transporters in plant cells: a brief review. Plants 9(8):967. https://doi.org/10.3390/plants9080967
Young G, Jack D, Smith D, Saier M (1999) The amino acid/auxin:proton symport permease family. Biochim Biophys Acta Biomembr 1415(2):306–322. https://doi.org/10.1016/S0005-2736(98)00196-5
Zdunek E, Lips SH (2001) Transport and accumulation rates of abscisic acid and aldehyde oxidase activity in Pisum sativum L. in response to suboptimal growth conditions. J Exp Bot 52(359):1269–1276. https://doi.org/10.1093/jexbot/52.359.1269
Zhang XD, Letham DS, Zhang R, Higgins TJV (1996) Expression of the isopentenyl transferase gene is regulated by auxin in transgenic tobacco tissues. Transg Res 5(1):57–65. https://doi.org/10.1007/BF01979922
Zhang X, Cui Y, Yu M, Su B, Gong W, Balu-íka F, Komis G, Sáamaj J, Shan X, Lin J (2019) Phosphorylation-mediated dynamics of nitrate transceptor NRT1.1 regulate auxin flux and nitrate signaling in lateral root growth1. Plant Physiol 181(2):480–498. https://doi.org/10.1104/pp.19.00346
Zhang H, Huo Y, Xu Z, Guo K, Wang Y, Zhang X, Xu N, Sun G (2020) Physiological and proteomics responses of nitrogen assimilation and glutamine/glutamine family of amino acids metabolism in mulberry (Morus alba L.) leaves to NaCl and NaHCO3 stress. Plant Signal Behav. https://doi.org/10.1080/15592324.2020.1798108
Zhao Y (2012) Auxin biosynthesis: a simple two-step pathway converts tryptophan to indole-3-acetic acid in plants. Mol Plant 5(2):334–338. https://doi.org/10.1093/mp/ssr104
Zhao L, Zhang W, Yang Y, Li Z, Li N, Qi S, Crawford NM, Wang Y (2018) The Arabidopsis NLP7 gene regulates nitrate signaling via NRT1.1-dependent pathway in the presence of ammonium. Sci Rep-UK. https://doi.org/10.1038/s41598-018-20038-4
Zhu A, Wang A, Zhang Y, Dennis ES, Peacock WJ, Greaves IK (2020) Early establishment of photosynthesis and auxin biosynthesis plays a key role in early biomass heterosis in Brassica napus (Canola) hybrids. Plant Cell Physiol 61(6):1134–1143. https://doi.org/10.1093/pcp/pcaa038
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Duarte-Aké, F., Márquez-López, R.E., Monroy-González, Z. et al. The source, level, and balance of nitrogen during the somatic embryogenesis process drive cellular differentiation. Planta 256, 113 (2022). https://doi.org/10.1007/s00425-022-04009-8
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DOI: https://doi.org/10.1007/s00425-022-04009-8