Abstract
Reproductive isolation poses a major obstacle to wide hybridization and introgression breeding of plants. Hybrid inviability in the postzygotic isolation barrier inevitably reduces hybrid fitness, consequently causing hindrances in the establishment of novel genotypes from the hybrids among genetically divergent parents. The idea that the plant immune system is involved in the hybrid problem is applicable to the intra- and/or interspecific hybrids of many different taxa. The lethality characteristics and expression profile of genes associated with the hypersensitive response of the hybrids, along with the suppression of causative genes, support the deleterious epistatic interaction of parental NB-LRR protein genes, resulting in aberrant hyper-immunity reactions in the hybrid. Moreover, the cellular, physiological, and biochemical reactions observed in hybrid cells also corroborate this hypothesis. However, the difference in genetic backgrounds of the respective hybrids may contribute to variations in lethality phenotypes among the parental species combinations. The mixed state in parental components of the chaperone complex (HSP90-SGT1-RAR1) in the hybrid may also affect the hybrid inviability. This review article discusses the facts and hypothesis regarding hybrid inviability, alongside the findings of studies on the hybrid lethality of interspecific hybrids of the genus Nicotiana. A possible solution for averting the hybrid problem has also been scrutinized with the aim of improving the wide hybridization and introgression breeding program in plants.
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Abbreviations
- CAPS:
-
Cleaved amplified polymorphic sequence
- CHORD1and 2:
-
Cysteine- and histidine-rich domain 1 and 2
- CRISPR-Cas9:
-
Clustered regularly interspaced short palindromic repeats-Cas9
- CS:
-
CHORD-containing protein and SGT1 domain
- EDS1:
-
Enhanced disease susceptibility 1
- HSP90:
-
Heat shock protein 90
- NB-LRR protein:
-
Nucleotide-binding site and leucine-rich repeat protein
- NLR protein:
-
NB and LRR–containing protein
- ND:
-
Nucleotide-binding domain
- RAR1:
-
Required for Mla 12 resistance
- SGS:
-
SGT1-specific domain
- SGT1:
-
Suppressor of G2 allele of Skp1
- SSR:
-
Simple sequence repeats
- TPR:
-
Tetratricopeptide repeat
- VIGS:
-
Virus-induced gene silencing
References
Aharon GS, Gelli A, Snedden WA, Blumwald E (1998) Activation of a plant plasma membrane Ca2+ channel by TGalpha 1, a heterotrimeric G protein alpha-subunit homologue. FEBS Lett 424:17–21. https://doi.org/10.1016/s0014-5793(98)00129-x
Aldon D, Mbengue M, Mazars C, Galaud J-P (2018) Calcium signalling in plant biotic interactions. Int J Mol Sci 19, 665; https://doi.org/10.3390/ijms19030665
Assmann SM (2002) Heterotrimeric and unconventional GTP binding proteins in plant cell signaling. Plant Cell 12:S355–S373. https://doi.org/10.1105/tpc.001792
Austin MJ, Muskett P, Kahn K, Feys BJ, Jones JDG, Parker JE (2002) Regulatory role of SGT1 in early R gene-mediated plant defenses. Science 295:2077–2080. https://doi.org/10.1126/science.1067747
Azevedo C, Sadanandom A, Kitagawa K, Freialdenhoven A, Shirasu K, Schulze-Lefert P (2002) The RAR1 interactor SGT1, an essential component of R gene-triggered disease resistance. Science 295:2073–2076. https://doi.org/10.1126/science.1067554
Azevedo C, Betsuyaku S, Peart J, Takahashi A, Noël L, Sadanandom A, Casais C, Parker J, Shirasu K (2006) Role of SGT1 in resistance protein accumulation in plant immunity. EMBO J 3:2007–1016. https://doi.org/10.1038/sj.emboj.7601084
Baack E, Melo MC, Rieseberg LH, Ortiz-Barrientos D (2015) The origins of reproductive isolation in plants. New Phytol 207:968–984. https://doi.org/10.1111/nph.13424
Baek YS, Covey PA, Petersen JJ, Chetelat RT, McClure B, Bedinger PA (2015) Testing the SI x SC rule: pollen-pistil interaction in interspecific crosses between members of the tomato clade (Solanum section Lycopersicon. Solanaceae). Am J Bot 102:302–311. https://doi.org/10.3732/ajb.1400484
Baggs E, Dagdas G, Krasileva KV (2017) NLR diversity, helpers and integrated domains: making sense of the NLR identity. Curr Opi Plant Biol 38:59–67. https://doi.org/10.1016/j.pbi.2017.04.012
Barragan AC, Weigel D (2021) Plant NLR diversity: the known unknowns of pan-NLRomes. Plant Cell 33:814–831. https://doi.org/10.1093/plcell/koaa002
Basso MF, Arraes FBM, Grossi-de-Sa M, Moreira VJV, Alves-Ferreira M, Grossi-de-Sa MF (2020) Insight into genetic and molecular elements for transgenic crop development. Front Plant Sci 11:509. https://doi.org/10.3389/fpls.2020.00509
Berbeć A, Doroszewska T (2020) The use of Nicotiana species in tobacco improvement. In: Ivanov NV, Sierro N, Peitsch MC (eds) The Tobacco Plant Genome, Compendium of Plant Genomes, Springer-Verlag, pp 101–146. https://doi.org/10.1007/978-3-030-29493-9
Bhaskar PB, Raasch JA, Kramer LC, Neumann P, Weilgus SM, Austin-Phillips S, Jiang J (2008) SgtI, but not RarI, is essential for the RB-medicated broad-spectrum resistance to potato late blight. BMC Plant Biol 8:8. https://doi.org/10.1186/1471-2229/8/8
Bindler G, Plieske J, Bakaher N, Gunduz I, Ivanov N, Van der Hoeven R, Ganal M, Donini P (2011) A high density genetic map of tobacco (Nicotiana tabacum L.) obtained from large scale microsatellite maker development. Theor Appl Genet 123:219–230. https://doi.org/10.1007/s00122-011-1578-8
Bomblies K, Lempe J, Epple P, Warthmann N, Lanz C, Dangl JL, Weigel D (2007) Autoimmune response as a mechanism for a Dobzhansky-Muller-type incompatibility syndrome in plants. PLoS Biol 5(9):2236. https://doi.org/10.1371/journal.pbil.0050236
Bomblies K, Weigel D (2007) Hybrid necrosis: autoimmunity as a potential gene-flow barrier in plant species. Nat Rev Genet 8:382–393. 10/1038/nrg2082
Bomlies K (2010) Doomed lovers: mechanism of isolation and incompatibility in plants. Annu Rev Plant Biol 61:109–124. https://doi.org/10.1146/annurev-arplant-042809-112146
Botër M, Amigues B, Peart J, Breuer C, Kadota Y, Casais C, Moore G, Kleanthous C, Ochsenbein F, Shirasu K, Guerois R (2007) Structural and functional analysis of SGT1 reveals that it interaction with HSP90 is required for the accumulation of Rx, and R protein involved in plant immunity. Plant Cell 19:3791–3804. https://doi.org/10.1105/tpc.107.050427
Bredow M, Monaghan J (2019) Regulation of plant immune signaling by calcium-dependent protein kinases. MPMI 32:6–19. https://doi.org/10.1094/MPMI-09-18-0267-FI
Broz AK, Bedinger PA (2021) Pollen-pistil interactions as reproductive barriers. Annu Rev Plant Biol 72:615–639. https://doi.org/10.1146/annurev-arplant-080620-102159
Calvo-Baltanás V, Wang J, Chae E (2021) Hybrid incompatibility of the plat immune system: an opposite force to heterosis equilibrating hybrid performances. Front Plant Sci 11:576796. https://doi.org/10.3389/fpls.2020.576796
Chase MW, Christenhusz MJM, Conran JG, Dodsworth S, de Assis FNM, Felix LP, Fay MF (2018) Unexpected diversity of Australian tobacco species (Nicotiana section Suaveolentes, Solanaceae). Curtis’s Bot Magaz 35:212–227. https://doi.org/10.1111/curt.12241
Chen C, Chen H, Lin Y-S, Shen J-B, Shan J-X, Qi P, Shi M, Zhu M-A, Huang X-H, Feng Q, Han B, Jiang L, Gao J-P, Lin H-X (2014) A two-locus interaction causes interspecific hybrid weakness in rice. Nat Commun 5:3357. https://doi.org/10.1038/ncomms4357
Chen H, Zhao Z, Liu L, Kong W, Lin Y, You S, Bai W, Xiao Y, Zheng H, Jiang L, Li J, Zhou J, Tao D, Wan J (2017) Genetic analysis of a hybrid sterility gene that causes both pollen and embryo sac sterility in hybrid between Oryza sativa L. and Oryza longistaminata. Heredity 119:166–173. https://doi.org/10.1038/hdy.2017.32
Chen J, Ding J, Ouyang Y, Du H, Yang J, Cheng K, Zhao J, Qui S, Zhang S, Yao J, Liu K, Wang L, Xu C, Li X, Xue Y, Xia M, Ji Q, Lu J, Xu M, Zhang Q (2008) A triallelic system of S5 is a major regulator of the reproductive barrier and compatibility of indica-japonica hybrid in rice. Proc Natl Acad Sci USA 105:11436–11441. https://doi.org/10.1073/pnas.0804761105
Cheval C, Aldon D, Galaud J-P, Ranty B (2013) Calcium/calmodulin-mediated regulation of plant immunity. Biochim Biophys Acta 1833:1766–1771. https://doi.org/10.1016/j.bbamcr.2013.01.031
Chung M-Y, Chung J-D, Ramanna M, van Tuyl JM, Lim K-B (2013) Production of polyploids and unreduced gametes in Lillum auratum × L. henryi hybrid. Int J Biol Sci 9:693–701. https://www.ijbs.com/v09p0693.htm
Clarkson JJ, Dodsworth S, Chase MW (2017) Time-calibrated phylogenetic trees establish a lag between polyploidization and diversification in Nicotiana (Solanaceae). Plant Syst Evol 303:1001–1012. https://doi.org/10.1007/s00606-017-1416-9
Coyne JA, Orr A (2004) Speciation. Sinauer Associates, Inc. Massachusetts U.S.A
Deng J, Fang L, Zhu X, Zhou B, Zhang T (2019) A CC-NBS-LRR gene induces hybrid lethality in cotton. J Exp Bot 70:5145–5156. https://doi.org/10.1093/jxb/erz312
DeVerna JW, Myers JR, Collins GB (1987) Bypassing prefertilization barriers to hybridization in Nicotiana using in vitro pollination and fertilization. Theor Appl Genet 73:665–671. https://doi.org/10.1007/BF00260773
Dongus JA, Parker JE (2021) EDS1 signalling: at the nexus of intracellular and surface receptor immunity. Curr Opin Plant Biol 62:102039. https://doi.org/10.1016/j.pbi.2021.102039
Durian G, Sedaghatmehr M, Matallana-Rmirex LP, Schilling SM, Schaepe S, Guerra T, Herde M, Whitte C-P, Mueller-Roeber B, Schulze WX, Balazadeh S, Romeis T (2020) Calcium-dependent protein kinase CPK1 controls cell death by in vivo phosphorylation of senescence master regulator ORE1. Plant Cell 32:1610–1625. https://doi.org/10.1105/tpc.19.00810
FAO, Food and Agricultural Organization of the United Nation (2011) Current status and options for crop biotechnologies in developing countries. Chapter 1 in proceedings of the FAO international technical conference on “Biotechnologies for agricultural development”. ISBN 978–92–5–106906–6
Filler DM, Luby JJ, Ascher PD (1994) Incongruity in the interspecific crosses of Vitis L. Morphological abnormalities in the F2 progeny. Euphytica 78:227–237. https://doi.org/10.1007/BF00027521
Fishman L, Sweigart AL (2018) When two rights make a wrong: the evolutionary genetics of plant hybrid incompatibilites. Annu Rev Plant Biol 69:701–731. https://doi.org/10.1146/annurev-arplant-042817-040113
Florez-Rueda AM, Paris M, Schmidt A, Widmer A, Grossniklaus U, Städler T (2016) Genomic inprinting in the endosperm is systematically perturbed in abortive hybrid tomato seeds. Mol Biol Evol 33:2935–2946. https://doi.org/10.1093/molbev/msw175
Fujii S, Tsuchimatu T, Kimura Y, Ishida S, Tangpranomkorn S, Shimosato-Asano H, Iwano M, Furukawa S, Itoyama W, Wada Y, Shimizu KK, Takayama S (2019) A stigmatic gene confers interspecies incompatibility in the Brassicaceae. Nature Plants 5:731–741. https://doi.org/10.1038/s41477-019-0444-6
Gerstel DU, Burns JA, Burk LG (1979) Interspecific hybridization with an African tobacco, Nicotiana africana Merxm. J Here 70:342–344. https://doi.org/10.1093/oxfordjournals.jhered.a109270
Goldsmith ZG, Dhanasekaran DN (2007) G protein regulation of MAPK networks. Oncogene 26:3122–3142. https://doi.org/10.1038/sj.onc.1210407
Gray WM, Muskett PR, Chunag H-W, Parker JE (2003) Arabidopsis SGT1b protein is required for SCFTIR1-mediated auxin response. Plant Cell 15:1310–1319. https://doi.org/10.1105/tpc.010884
Halterman DA, Wise RP (2004) A single-amino acid substitution in the sixth leucine-rich repeat of barley MLA6 and MLA13 alleviates dependence of RAR1 for disease resistance signaling. Plant J 38:215–226. https://doi.org/10.1111/j.1365-313X.2004.02302.x
Hancock WG, Kuraparthy V, Kernodle SP, Lewis RS (2015) Identification of maternal haploids of Nicotiana tabacum aided by transgenic expression of green fluorescent protein: evidence for chromosome elimination in the N. tabacum × N. africana interspecific cross. Mol Breed 35:179. https://doi.org/10.1007/s11032-015-0372-8
Hann DR, Rathjen JP (2007) Early events in the pathogenicity of Pseudomonas syringae on Nictiana benthamiana. Plant J 49:607–618. https://doi.org/10.111/j.1365-313X.2006.02981.x
Hermsen JGTH (1963) Hybrid necrosis as a problem for the wheat breeder. Euphytica 12:1–16. https://doi.org/10.1007/BF00033587
Hondnett GL, Burson BL, Rooney WL, Dillon SL, Price HJ (2005) Pollen-Pistil Interaction Result in Reproductive Isolation between Sorghum Bicolor and Divergent Sorghum. Species 45:1403–1409. https://doi.org/10.2135/cropsci2004.0429
Ibañez MS, Camadro EL (2015) Reproductive behavior of the wild carrots Daucus pusillus and Daucus montanus from Argentina. Botany 93:279–286. https://doi.org/10.1139/cjb-2014-0243
Iizuka T, Kuboyama T, Marubashi W, Oda M, Tezuka T (2012) Nicotiana debneyi has a single dominant gene causing hybrid lethality in crosses with N. tabacum. Euphytica 186:321–328. https://doi.org/10.1007/s10681-011-0570-3
Inoue E, Marubashi W, Niwa M (1996) Genomic factors controlling the lethality exhibited in the hybrid between Nicotiana suaveolens Lehm. and N. tabacum L. Theor Appl Genet 93:341–347. https://doi.org/10.1007/BF00223174
Jeuken MJW, Zhang NW, McHale L, Pelgrom K, den Boer E, Lindhout P, Michelmore RW, Visser RGF, Niks R (2009) Rin4 causes hybrid necrosis and race-specific resistance in an interspecific lettuce hybrid. Plant Cell 21:3368–3378. https://doi.org/10.1105/tpc.109.070334
Jhaveri K, Taldone T, Modi S, Chiosis G (2012) Advances in the clinical development of heat shock protein 90 (Hsp90) inhibitors in cancers. Biochimi Biophys Acta 1823:742–755. https://doi.org/10.1016/j.bbamcr.2011.10.008
Jones JDG, Dangle JL (2006) The plant immune system. Nature 444:323–329. https://doi.org/10.1038/nature05286
Junghee HJ, Wang S, Chen JG, Jones AM, Fedoroff NV (2005) Different signaling and cell death roles of heterotrimeric G protein a and b subunits in the Arabidopsis oxidative stress response to ozone. Plant Cell 17:957–970. https://doi.org/10.1105/tpc.104.029603
Kadota Y, Shirasu K (2012) The HSP90 complex of plants. Biochimi Biophys Acta 1823:689–697. https://doi.org/10.1016/j.bbamcr.2011.09.016
Kagawa F (1957) Crop breeding based on the interspecific and intergeneric hybridization (Japanese title to English translation). in Japanese, Sangyo Tosho Co. Ltd
Katsuyama Y, Doi M, Shioya S, Hane S, Yoshioka M, Date S, Miyahara C, Ogawa T, Takada R, Okumura H, Ikusawa R, Kitajima S, Oda K, Sato K, Tanaka Y, Tezuka T, Mino M (2021) The role of chaperone complex HSP90-SGT1-RAR19 as the associated machinery for hybrid inviability between Nicotiana gossei Domin and N. tabacum L. Gene 776:145443. https://doi.org/10.1016/j.gene.2021.145443
Kawaguchi K, Ohya Y, Maekawa M, Iizuka T, Hasegawa A, Shiragaki K, He H, Oda M, Morikawa T, Yokoi S, Tezuka T (2021) Two Nicotiana occidentalis accessions enable gene identification for type II hybrid lethality by the cross to N. sylvestris. Sci Rep 11:17093. https://doi.org/10.1038/s41598-021-96482-6
Kelly LJ, Leitch AR, Clarkson JJ, Knapp S, Chase MW (2012) Reconstructing the complex evolutionary origin of wild allopolyploid tobacco (Nicotiana section Suaveolentes). Evolution 67:80–94. https://doi.org/10.1111/j.1558-5646.2012.01748.x
Kermicle JL (2006) A selfish gene governing pollen-pistil compatibility confers reproductive isolation between maize relatives. Genet 172:499–506. https://doi.org/10.1534/genetics.105.048645
Kobori S, Masuda Y, Marubashi W (2005) Heat treatment temporarily suppresses expression of programmed cell death in hybrid tobacco cells (Nicotiana suaveolens x N. tabacum) expressing hybrid lethality. Plant Biotec 22:345–348. https://doi.org/10.5511/plantbiotechnology.22.345
Krüger J, Thomas CM, Golstein C, Dixon S, Smoker M, Tang S, Mulder L, Jones JDG (2002) A tomato cysteine protease required for Cf-2-dependent disease resistance and suppression of autonecrosis. Science 296:744–747. https://doi.org/10.1126/science.1069288
Kumar D, Kirti PB (2015) Pathogen-induced SGT1 of Arachis diogoi induces cell death and enhanced disease resistance in tobacco and peanut. Plant Biotech J 13:73–84. https://doi.org/10.1111/pbi.12237
Kurusu T, Kuchitsu K, Tada Y (2015) Plant signaling networks involving Ca2+ and Rboh/Nox-mediated ROS production under salinity stress. Front Plant Sci 6:427. https://doi.org/10.3389/fpls.2015.00427
Lafon-Placette C, Johannessen IM, Hornslien KS, Ali MF, Bjerkan KN, Bramsiepe J, Glöckle BM, Rebernig CA, Brysting AK, Grini P, Köhler C (2017) Endosperm-based hybridization barriers explain the pattern of gene flow between Arabidopsis lyrate and Arabidopsis arenosa in central Europe. Proc Ntl Acd Sci USA 114:E1027-E1035. https://www.pnas.org/content/114/6/E1027
Lefevere H, Bauters L, Gheysen G (2020) Salicylic acid biosynthesis in plants. Frot Plant Sci 11:228. https://doi.org/10.3389/fpls.2020.00338
Leister D (2004) Tandem and segmental gene duplication and recombination in the evolution of plant resistance gene. Trend Genet 20:116–122. https://doi.org/10.1016/j.tig.2004.01.007
Li D, Chen L, Jiang L, Zhu S, Zhao Z, Liu S, Su N, Zhai H, Ikehashi H, Wan J (2007) Fine mapping of S32(t), a new gene causing hybrid embryo sac sterility in a Chinese landrace rice (Oryza sativa L.) Theor Appl Genet 114:515–524. https://doi.org/10.1007/s00122-006-0450-8
Li J, Zhou J, Zhang Y, Yang Y, Pu Q, Tao D (2020) New insights into the nature of interspecific hybrid sterility in rice. Front Plant Sci 11:555572. https://doi.org/10.3389/fpls.2020.555572
Li L, Liu B, Deng S, Zhao H, Li H, Xing S, Fetzer DD, Li M, Nasrallah ME, Nasrallah JB, Liu P (2018) Evolution of interspecies unilateral incompatibility in relatives of Arabidopsis thaliana. Mol Ecol 27:2742–2753. https://doi.org/10.1111/mec.14707
Liu Y, Hokin SA, Kermicle JL, Hartwig T, Evans MM (2019) A pistil-expressed pectin methylesterase confers cross-incompatibility between strains of Zea mays. Nature Commun 10:2304. https://doi.org/10.1038/s41467-019-10259-0
Ma J, Hancock WG, Nifong JM, Kernodle SP, Lewis RS (2020) Identification and editing of a hybrid lethality gene expands the range of interspecific hybridization potential in Nicotiana. Theor Appl Genet 133:2915–2925. https://doi.org/10.1007/s00122-020-03641-w
Marcellán ON, Camadro EL (1996) Self- and cross-incompatibility in Asparagus officinalis and Asparagus densiflorus cv. Sprengeri Can J Bot 74:1621–1625. https://doi.org/10.1139/b96-196
Marubashi W, Yamada T, Niwa M (1999) Apoptosis detected in hybrids between Nicotiana glutinosa and N. repanda expressing lethality. Planta 210:168–171. https://doi.org/10.1007/s004250050667
Marubashi W, Onosato K (2002) Q chromosome controls the lethality of interspecific hybrids between Nicotiana tabacum and N. suaveolens. Breed Sci 52:137–142. https://doi.org/10.1270/jsbbs.52.137
Marubashi W, Kobayashi M (2002) Temperature-dependent apoptosis detected in the hybrid between Nicotiana debneyi and N. tabacum expressing lethality. Plant Biotec 19:267–270. https://doi.org/10.5511/plantbiotechnology.19.267
Masuda Y, Yamada T, Marubashi W (2003) Time course analysis of apoptosis during hybrid lethality in tobacco hybrid cell (Nicotiana suaveolens x N. tabacum). Plant Cell Physiol 44:420–427. https://doi.org/10.1093/pcp/pcg055
Masuda Y, Yamada T, Kuboyama T, Marubashi W (2007) Identification and characterization of gene involved in hybrid lethality in hybrid tobacco cells (Nicotiana suaveolens × N. tabacum) using suppression subtractive hybridization. Plant Cell Rep 26:1595–1604. https://doi.org/10.1007/s00299-007-0352-5
Maune JF, Camadro EL, Erazzú LE (2018) Cross-incompatibility and self-incompatibility: unrelated phenomena in wild and cultivated potatoes? Botany 96:33–45. https://doi.org/10.1139/cjb-2017-0070
Mcllwain DR, Berger T, Mak TW (2013) Caspase functions in cell death and disease. Cold Spring Harb Perspect Biol 3(5):a008656. https://doi.org/10.1101/cshperspect.a008656
Melo MC, Grealy A, Brittain B, Walter GM, Ortiz-Barrientos D (2014) Strong extrinsic reproductive isolation between parapatric populations of an Australian groundsel. New Phytol 203:323–334. https://doi.org/10.1111/nph.12779
Mergoum M, Sapkota S, ElDoliefy AEA, Naraghi, SM, Pirseyedi S, Alamri SM, AbuHammad W (2019) Triticale (x Triticosecale Wittmarck) breeding. In: Al-Khayri JM, Jain M, Johnson DV (Eds) Advances in Plant Breeding Strategies: Cereals. Springer Verlag. Chapter 11 pp405–451
Mestre P, Baulcombe DC (2006) Elicitor-medicated oligomerization of the tobacco N disease resistance protein. Plant Cell 18:491–501. https://doi.org/10.1105/tpc.105.037234
Miles GP, Samuel MA, Jones AM, Ellis E (2004) Mastoparan rapidly activates plant MAP kinase signaling independent of heterotrimeric G proteins. Plant Physiol 134:1332–1336. https://doi.org/10.1104/pp.103.037275
Mino M, Maekawa K, Ogawa K, Yamagishi H, Inoue M (2002) Cell death processes during expression of hybrid lethality in interspecific hybrid between Nicotiana gossei Domin and Nicotiana tabacum L. Plant Physiol 130:1776–1787. https://doi.org/10.1104/pp.006023
Mino M, Abe S, Suzuki T, Yokoyama H, Kaminaka H, Ogawa K, Morita S, Masumura T, Tnaka K, Inoue M (2004) Hydrogen peroxide functions as a cell death signal for hybrid lethality in the F1 of Nicotiana gossei × N. tabacum. Plant Sci 167:267–274. https://doi.org/10.1016/j.plantsci.2004.03.028
Mino M, Misaka Y, Ueda J, Ogawa K, Inoue M (2005) Hybrid lethality of cultured cells of an interspecific F1 hybrid of Nicotiana gossei Domin and N. tabacum L. Plant Cell Rep 24:179–188. https://doi.org/10.1007/s00299-005-0923-2
Mino M, Kubota M, Yamaguchi Y, Kawamori T, Sato K, Misaka Y, Tanaka Y, Inoue M (2006) Searching for genetic factors involved in hybrid lethality in Nicotiana; possible use of a cultured cell line of a hybrid. Plant Biotech 23:487–492. https://doi.org/10.5511/plantbiotechnology.23.487
Mino M, Kubota M, Nogi T, Zhang S, Inoue M (2007a) Hybrid lethality in interspecific F1 hybrid N. gossei x N. tabacum involves a MAP-kinase signaling cascade. Plant Biol 9:366–373. https://doi.org/10.1055/s-2006-924725
Mino M, Murata N, Date S, Inoue M (2007b) Cell death in seedling of the interspecific hybrid Nicotiana gossei and N. tabacum; possible role of knob-like bodies formed on tonoplast in vacuolar-collapse-mediated cell death. Plant Cell Rep 26:407–419. https://doi.org/10.1007/s00299-006-0261-z
Mizuno N, Hosogi N, Park P, Takumi S (2010) Hypersensitive response-like reaction is associated with hybrid necrosis in interspecific crosses between tetraploid wheat and Aegilops tauschii cross. PLoS ONE 5(6):e11326. https://doi.org/10.1371/journal.pone.0011326
Mizuno N, Shitsukawa N, Hosogi N, Park P, Takumi S (2011) Autoimmune response and repression of mitotic cell division occur in inter-specific crosses between tetraploid wheat and Aegilops tauschii Coss. that show low temperature-induced hybrid necrosis. Plant J 68:114–128. https://doi.org/10.1111/j.1365-313X.2011.04667.x
Montanari S, Brewer L, Lamberts R, Velasco R, Malonoy M, Perchepied L, Guérif P, Durel C-E, Bus VGM, Gardiner S, Chagné D (2016) Genome mapping of postzygotic hybrid necrosis in an interspecific pear population. Horticulture Res 3:15064. https://doi.org/10.1038/hortres.2015.64
Morel J-B, Dangl JL (1997) The hypersensitive response and the induction of cell death in plant. Cell Death Differ 4:671–683. https://doi.org/10.1038/sj.cdd.4400309
Moyle LC, Nakazato T (2008) Comparative genetics of hybrid incompatibility: sterility in two Solanum species crosses. Genet 179:1437–1453. https://doi.org/10.1534/genetics.107.083618
Müller LM, Lindner H, Pires ND, Gagliardini V, Grossniklaus V (2016) A subunit of the oligosaccharyltransferase complex is required for interspecific gametophyte recognition in Arabidopsis. Nat Commun 7:10826. https://doi.org/10.1038/ncomms10826
Muskett PR, Kahn K, Austin MJ, Moisan LJ, Sadanandom A, Shirasu K, Jones JD, Parker JE (2002) Arabidopsis RAR1 exerts rate-limiting control of R gene-medicated defenses against multiple pathogens. Plant Cell 14:979–992. https://doi.org/10.1105/tpc.001040
Nakata K, Nagashima H, Inaba N, Yamashita H, Shinozaki Y, Kanekatsu M, Marubashi W, Yamada T (2021) Analysis of the possible cytogenetic mechanism for overcoming hybrid lethality in an interspecific cross between Nicotiana suaveolens and Nicotiana tabacum. Sci Rep 11:7812. https://doi.org/10.1038/s41598-021-87242-7
Ogasawara Y, Kaya H, Hiraoka G, Yumoto F, Kimura S, Kadota Y, Hishinuma H, Senzaki E, Yamagoe S, Nagata K, Nara M, Suzuki K, Tanokura M, Kuchitsu K (2008) Synergistic activation of the Arabidopsis NADPH oxidase AtrbohD by Ca2+ and phosphorylation. J Biol Chem 283:8885–8892. https://doi.org/10.1074/jbc.M708106200
Oka H (1974) Analysis of genes controlling F1 sterility in rice by the use of isogenic lines. Genet 77:521–534. https://doi.org/10.1093/genetics/77.3.521
Oneal F, Willis JH, Franks RG (2016) Disruption of endosperm development is a major cause of hybrid seed inviability between Mimulus guttatus and Mimulas nudatus. New Phytol 210:1107–1120. https://doi.org/10.1111/nph.13842
Onus AN, Pickersgill B (2004) Unilateral incompatibility in Capsicum (Solanaceae): occurrence and taxonomic distribution. Ann Bot 94:289–295. https://doi.org/10.1093/aob/mch139
Ouyang Y, Zhang Q (2013) Understanding reproductive isolation based on the rice model. Annu Rev Plant Biol 64:111–135. https://doi.org/10.1146/annurev-arplant-050312-120205
Ouyang Y, Zhang Q (2018) The molecular and evolutionary basis of reproductive isolation in plants. J Genet Genomics 45:613–620. https://doi.org/10.1016/j.jgg.2018.10.004
Pedley KF, Martin GB (2005) Role of mitogen-activated protein kinases in plant immunity. Curr Opin Plant Biol 8:541–547. https://doi.org/10.1016/j.pbi.2005.07.006
Pieterse CM, Van der Does D, Zamioudis C, Leon-Reyes A, Van Wees SCM (2012) Hormonal modulation of plant immunity. Annu Rev Cell Dev Biol 28:489–521. https://doi.org/10.1146/annurev-cellbio-092910-154055
Pramanik K, Sahoo JP, Mohapatra PP, Acharya LK, Jena C (2021) Insight into the embryo rescue – a modern in-vitro crop improvement approach in horticulture. Plant Cell Biotech Mol Biol 22:20–33. https://www.ikprress.org/index.php/PCBMB/article/view/6025
Ram SG, Sundaravelpandian K, Kumar M, Vinod KK, Bapu JRK, Raveendran TS (2006) Pollen-pistil interaction in the inter-specific crosses of Sesamum sp. Euphytica 152:379–385. https://doi.org/10.1007/s10681-006-9225-1
Reddy ASN, Ali GS, Celesnik H, Day LS (2011) Coping with stresses: roles of calcium-and calcium/calmodulin-regulated gene expression. Plant Cell 23:2010–2032. https://doi.org/10.1105/tpc.111.084988
Ren H, Zhao X, Li W, Hussain J, Qi G, Liu S (2021) Calcium signaling in plant programmed cell death. Cells 10:1089. https://doi.org/10.3390/cells10051089
Ren ZL, Lelley T (1988) Genetics of hybrid necrosis in rye. Plant Breed 100:173–180. https://doi.org/10.1111/j.1439-0523.1988.tb00237.x
Sanchez-Ramos JR (2020) The rise and fall of tobacco as a botanical medicine. J Herbal Med 22:100374. https://doi.org/10.1016/j.hermed.2020.100374
Schuster M (2000) Genetics of powdery mildew resistance in Malus species. Acta Hort 538:593–595. https://doi.org/10.17660/ActaHortic.2000.538.103
Sheen J (1996) Ca2+-dependent protein kinases and stress signal transduction in plants. Science 274:1900–1902. https://doi.org/10.1126/science.274.5294.1900
Shiragaki K, Nakamura R, Nomura S, He H, Yamada T, Marubashi W, Oda M, Tezuka T (2020) Phenylalanine ammonia-lyase and phenolic compounds are related to hybrid lethality in the cross Nicotiana suaveolens x N. tabacum. Plant Biotec 37:327–333. https://doi.org/10.5511/plantbiotechnology.20.0606a
Shirasu K, Lahaye T, Tan M-W, Zhou F, Azevedo C, Schultze-Lefert P (1999) A novel class of eukaryotic zinc-binding proteins is required for disease resistance signaling in barley and development in C. elegans. Cell 99:355–366. https://doi.org/10.1016/s0092-8674(00)81522-6
Shirasu K (2009) The HSP90-SGT1 chaperone complex for NLR immune sensors. Annu Rev Plant Biol 60:139–164. https://doi.org/10.1146/annurev.arplant.59.032607.092906
Sicard A, Kappel C, Josephs EB, Lee YW, Marona C, Stinchcombe JR, Wright SI, Lenhard M (2015) Divergent sorting of a balanced ancestral polymorphism underlies the establishment of gene-flow barriers in Capsella. Nat Commun 6:7960. https://doi.org/10.1038/ncomms8960
Simon M, Durand S, Pluta N, Gobron N, Botran L, Ricou A, Camilleri C, Budar F (2016) Genomic conflicts that cause pollen mortality and raise reproductive barriers in Arabidopsis thaliana. Genet 203:1353–1367. https://doi.org/10.1534/genetics.115.183707
Singh DP, Singh AK, Singh A (2021) Wide hybridization (chapter 6) in plant breeding and cultivar development. Academic Press. ISBN 978–0–12–817563–7
Song M-Y, Kim C-Y, Han M, Ryu H-S, Lee S-K, Sun L, He Z, Seo Y-S, Canal P, Ronald PC, Jeon J-S (2013) Differential requirement of Oryza sativa RAR1 in immune receptor-mediated resistance of rice to Magnaporthe oryzae. Mol Cells 35:327–334. https://doi.org/10.1007/s10059-013-2317-6
Song X, Qui SQ, Xu GG, Li XH, Zhang Q (2005) Genetic dissection of embryo sac fertility, pollen fertility, and their contributions to spikelet fertility of intersubspecific hybrids in rice. Theor Appl Genet 110:205–211. https://doi.org/10.1007/s00122-004-1798-2
Staal J, Kaliff M, Bohman S, Dixelius C (2006) Transgressive segregation reveals two Arabidopsis TIR-NB-LRR resistance genes effective against Leptosphaeria maculans, causal agent of blackleg disease. Plant J 46:18–30. https://doi.org/10.1111/j.1365-313X.2006.02688.x
Stebbins GL (1971) Chromosomal changes, genetic recombination, and speciation (chapter 4) in chromosomal evolution in higher plants. Edward Arnold Ltd., London, pp 72–123
Storme ND, Mason A (2014) Plant speciation through chromosome instability and ploidy change: cellular mechanisms, molecular factors and evolutionary relevance. Curr Plant Biol 1:10–33. https://doi.org/10.1016/j.cpb.2014.09.002
Suharsono U, Fijisawa Y, Kawasaki T, Iwasaki Y, Satoh H, Shimamoto K (2002) The heterotrimeric G protein a subunit acts upstream of the small GTPase rac in disease resistance of rice. Proc Natl Acad Sci USA 99:13307–13312. https://doi.org/10.1073/pnas.192244099
Sweigart A, Flagel LE (2015) Evidence of natural selection acting on a polymorphic hybrid incompatibility locus in Mimulus. Genet 199:543–554. https://doi.org/10.1534/genetics.114.171819
Szymajd M, Napiórkowska B, Korbin M, Żurawicz E (2015) Studies on the interspecific crossing compatibility among three Prunus species and their hybrids. Hort Sci 42:70–82. https://doi.org/10.17221/273/2014-HORTSCI
Takahashi A, Casais C, Ichimura K, Shirasu K (2003) HSP90 interacts with RAR1 and SGT1 and is essential for RPS2-medicated disease resistance in Arabidopsis. Proc Natl Acad Sci USA 100:11777–11782. https://doi.org/10.1073/pnas.2033934100
Tezuka T, Marubashi W (2006) Hybrid lethality in interspecific hybrids between Nicotiana tabacum and N. suaveolens: evidence that Q chromosome cause hybrid lethality based on Q-chromosome-specific DNA markers. Theor Appl Genet 112:1172–1178. https://doi.org/10.1007/s00122-006-0219-0
Tezuka T, Kuboyama T, Matsuda T, Maarubashi W (2007) Possible involvement of genes on the Q chromosome of Nicotiana tabacum in expression of hybrid lethality and programmed cell death during interspecific hybridization to N. debneyi. Planta 226:753–764. https://doi.org/10.1007/s00425-007-0522-2
Tezuka T, Kuboyama T, Matsuda T, Marubashi W (2010) Seven of eight species in Nicotiana section Suaveolentes have common factors leading to hybrid lethality in crosses with Nicotiana tabacum. Ann Bot 106:267–276. https://doi.org/10.1093/aob/mcq114
Tezuka T, Marubashi W (2012) Genes in S and T subgenomes are responsible for hybrid lethality in interspecific hybrids between N. tabacum and N. occidentalis. PLoS ONE 7(4): e36204. https://doi.org/10.1371/journal.pone.0036204
Tezuka T, Matsuo C, Iizuka T, Oda M, Marubashi W (2012) Identification of Nicotiana tabacum linkage group corresponding to the Q chromosome gene(s) involved in hybrid lethality. PLoS ONE 7(5):e37822. https://doi.org/10.1371/journal.pone.0037822
Tezuka T, Kitamura N, Imagawa S, Hasegawa A, Siragaki K, He H, Yanase M, Ogata Y, Morikawa T, Yokoi S (2021) Genetic mapping of the HLA1 locus causing hybrid lethality in Nicotiana interspecific hybrids. Plants 10(10):2062. https://doi.org/10.3390/plants10102062
Tornero P, Merritt P, Sadanandom A, Shirasu K, Innes RW, Dangl J (2002) RAR1 and NDR1 contribute quantitatively to disease resistance in Arabidopsis, and their relative contributions are dependent on the R gene assayed. Plant Cell 14:1005–1015. https://doi.org/10.1105/tpc.001032
Tran DTN, Chung E-H, Harbring-Müller A, Demar M, Schwab R, Dangle JL, Weigel D, Chae E (2017) Activation of a plant NLR complex through heteromeric association with an autoimmune risk variant of another NLR. Curr Biol 27:1148–1160. https://doi.org/10.1016/j.cub.2017.03.018
Ueno N, Nihei S, Miyakawa N, Hirasawa T, Kanekatsu M, Marubashi W, van Doorn WG, Yamada T (2016) Time course of programmed cell death, which induced autophagic features, in hybrid tobacco cell expressing hybrid lethality. Plant Cell Rep 35:2475–2488. https://doi.org/10.1007/s00299-016-2048-1
Valkonen JPT, Watanabe KN (1999) Autonomous cell death, temperature sensitivity and the genetic control associated with resistance to cucumber mosaic virus (CMV) in diploid potatoes (Solanum spp.). Theor Appl Genet 99:996–1005. https://doi.org/10.1007/s001220051407
Valmonte GR, Arthur K, Higgins CM, MacDiarmid M (2014) Calcium-dependent protein kinase in plants: evolution, expression and function. Plant Cell Physiol 55:551–569. https://doi.org/10.1093/pcp/pct200
von Wettberg E, Davis TM, Smýkal P (2020) Editorial: wild plants as source of new crops. Front Plant Sci 11:591554. https://doi.org/10.3389/fpls.2020.591554
Wan J, Yamaguchi Y, Kato H, Ikehashi H (1996) Two new loci for hybrid sterility in cultivated rice (Oryza sativa L.). Theor Appl Genet 92:183–190. https://doi.org/10.1007/BF00223375
Wang GF, Fan R, Wang X, Wang D, Zhang X (2015) TaRAR1 and TaSGT1 associate with TaHsp90 to function in bread wheat (Triticum aestivum L.) seedling growth and stripe rust resistance. Plant Mol Biol 87:577–589. https://doi.org/10.1007/s11103-015-0298-x
Wang GW, He YQ, Xu GG, Zhang Q (2006) Fine mapping of f5-Du, a gene conferring wide-compatibility for pollen fertility in inter-subspecific hybrid of rice (Oryza sativa L.). Theor Appl Genet 112:382–387. https://doi.org/10.1007/s00122-005-0141-x
Wang H, Ren Y, Zhou J, Du J, Hou J, Jiang R, Wang H, Tian Z, Xie C (2017) The cell death triggered by the nuclear localized RxLR effector PITG_22798 from Phytophthora infestans is suppressed by the effector AVR3b. Int J Mol Sci 18:409. https://doi.org/10.3390/ijms18020409
Wang K, Uppalapati SR, Zhu X, Dinesh-Kumar SP, Mysore KS (2010) SGT1 positively regulates the process of plant cell death during both compatible and incompatible plant-pathogen interactions. Mol Plant Patho 11:597–611. https://doi.org/10.1111/j.1364-3703.2010.00631.x
Wang L, Zhao L, Zhang X, Zhang Q, Jia Y, Wang G, Li S, Tian D, Li W-H, Yang S (2019) Large-scale identification and functional analysis of NLR genes in blast resistance in the Tetep rice genome sequence. Proc Natl Acad Sci USA 116:18479–18487. https://doi.org/10.1073/pnas.1910229116
Wang Y, Gao M, Li Q, Wang L, Wang J, Jeon J-S, Qu N, Zhang Y, He Z (2008) OsRAR1 and OsSGT1 physically interact and function in rice basal disease resistance. Mol Plant-Microbe Interact 21:294–303. https://doi.org/10.1094/MPMI-21-3-0294
Warren RF, Merritt PM, Holub E, Innes RW (1999) Identification of three putative signal transduction gene involved in R gene-specified disease resistance in Arabidopsis. Genet 152:401–412. https://doi.org/10.1093/genetics/152.1.401
Woltering EJ (2004) Death protease come alive. Trend Plant Sci 9:469–472. https://doi.org/10.1016/j.tplants.2004.08.001
Wu D-H, Abd-El-Haliem A, Bozkurt TO, Belhaj K, Terauchi R, Vossen JH, Kamoun S (2017) NLR network mediates immunity to diverse plant pathogens. Proc Natl Acad Sci USA 114:8113–8118. https://doi.org/10.1073/pnas.1702041114
Xiao Z, Hu Y, Zhang X, Xue Y, Fang Z, Yang L, Zhang Y, Liu Y, Li Z, Liu X, Liu Z, Lv H, Zhung M (2017) Fine mapping and transcriptome analysis reveal candidate gene associated with hybrid lethality in cabbage (Brassica oleracea). Genes 8:147. https://doi.org/10.3390/genes8060147
Xing L, Qian C, Cao A, Li Y, Jiang Z, Li M, Jin X, Hu J, Zhang Y, Wang X, Chen P (2013) The Hv-SGT1 gene from Haynaldia villosa contributes to resistance toward both biotrophic and hemi-biotrophic pathogens in common wheat (Triticum aestivum). PLoS ONE 8:e72571. https://doi.org/10.1371/journal.pone.0072571
Yamada T, Marubashi W, Niwa M (1999) Detection of four lethality types in interspecific crosses among Nicotiana species through the use of three rescue methods for lethality. Breed Sci 49:203–210. https://doi.org/10.1270/jsbbs.49.203
Yamada T, Marubashi W, Niwa M (2000) Apoptotic cell death induced temperature-sensitive lethality expressed in hybrid seedlings and calli derived from the cross of Nicotiana suaveolens x N. tabacum. Planta 211:614–622. https://doi.org/10.1007/s004250000329
Yamada T, Marubashi W, Niwa M (2001) Facile induction of apoptosis into plant cell associated with temperature-sensitive lethality shown on interspecific hybrid from the cross Nicotiana suaveolens x N. tabacum. Plant Cell Physiol 42:203–213
Yamada T, Marubashi W (2003) Over-produced ethylene causes apoptotic cell death leading to temperature-sensitive lethality in hybrid seedlings from the cross of Nicotiana suaveolens x N. tabacum. Planta 217:690–698. https://doi.org/10.1007/s00425-003-1035-2
Yamamoto E, Takashi T, Morinaka Y, Lin S, Wu J, Matsumoto T, Kitano H, Matsuoka M, Ashikari M (2010) Gain of deleterious function causes an autoimmune response and Bateson-Dobzhansky-Muller incompatibility in rice. Mol Genet Genomics 283:305–315. https://doi.org/10.1007/s00438-010-0514-y
Yamamoto T, Shomura S, Mino M (2017) Cell physiology of mortality and immortality in a Nicotiana interspecific F1 hybrid complies with the quantitative balance between reactive oxygen and nitric oxide. J Plant Physiol 210:72–83. https://doi.org/10.1016/j.jplph.2017.01.001
Yanagihara S, Kato H, Ikehashi H (1992) A new locus for multiple alleles causing hybrid sterility between an Aus variety and javanica varieties in rice (Oryza sativa L.). Jpn J Breed 42:793–801
Yang K-Y, Liu Y, Zhang S (2001) Activation of a mitogen-activated protein kinase pathway is involved in disease resistance in tobacco. Proc Natl Acad Sci USA 98:741–745. https://doi.org/10.1073/pnas.98.2.741
Yu X, Zhao Z, Zheng X, Zhou J, Kong W, Wang P, Bai W, Zheng H, Zhang H, Li J, Liu J, Wang Q, Zhang L, Liu K, Yu Y, Guo X, Wang J, Lin Q, Wu F, Ren Y, Zhu S, Ahang X, Cheng Z, ei C, Liu S, Siu X, Tian Y, Jiang L, Ge S, Wu C, Tao D, Wang H, Wan J, (2018) A selfish genetic element confers non-Mendelian inheritance in rice. Science 360:1130–1132. https://doi.org/10.1126/science.aar4279
Yuan C, Li C, Zhao X, Yan C, Wang J, Mou Y, Sun Q, Shan S (2021) Genome-wide identification and characterization of HSP90-RAR1-SGT1-complex members from Arachis genomes and their responses biotic and abiotic stresses. Front Genet 12:689669. https://doi.org/10.3389/fgene.2021.689669
Zhang L, Chen Q, Yuan Z, Xiang Z, Sheng Y, Liu D (2008) Production of aneuhaploid and euhaploid sporocytes by meiotic restitution in fertile hybrid between durum wheat Langdon chromosome substitution line and Aegilops tauschii. J Gene Genomics 35:617–623. https://doi.org/10.1016/S1673-8527(08)60082-x
Zhao Z, Wang C, Jiang L, Zhus S, Ikehashi H, Wan J (2006) Identification of a new hybrid sterility gene in rice (bi Oryza sativa L.). Euphytica 151:331–337. https://doi.org/10.1007/s10681-006-9154-z
Zhu SS, Wang CM, Zheng TQ, Ikehashi H, Wan J (2005) A new gene located on chromosome 2 causing hybrid sterility in a remote cross of rice. Plant Breed 124:440–445. https://doi.org/10.1111/j.1439-0523.2005.01143.x
Acknowledgements
We are indebted to Mr. Takumi Yamamoto for his contribution to collect a part of the data in Fig. 3. This study did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
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Masanobu Mino, the corresponding author, certifies that all authors have participated sufficiently in preparing the manuscript. Masanobu Mino gave the basic idea for the article, performed the literature search, wrote manuscript, and reviewed and edited the manuscript. Takahiro Tezuka proposed ideas for improving the quality of the article and reviewed and edited the manuscript. Sachiko Shomura performed the experiments, collected and analyzed the data in Figs. 2 and 3, and reviewed the manuscript.
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Appendices
Appendix 1
Table 1
Appendix 2
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1.
Cell culture and determination of cell viability
After 3 to 4 days of subculture in fresh liquid medium, the cells were transferred to 26 ºC or 37 ºC, and their viability was determined by a previously reported method (Mino et al. 2005).
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2.
Cellular treatment
The pharmacological treatments of the cells were performed 0.5 h before transferring the cells from 37 ºC to 26 ºC. Cell viability was determined 3 h following the temperature shift. Moreover, to explore the effects of calcium ion (Ca2+), the cells were cultured for 10 days in the calcium-free medium to reduce intracellular Ca2+ concentration. The concentration of each reagent treatment was as follows: okadaic acid (OkA), 0.1 μM; calyculin A (CA), 0.1 μM; staurospolin (ST), 1 μM; U0126, 100 μM; mastoparan (MP), 5 μM; gadolinium chloride (GD), 5 μM; ruthenium red (Rred), 50 mM; ethylene glycol tetraacetic acid (EGTA), 1 mM; CaCl2 (Ca), 1 mM; and neomycine (Neo), 100 μM.
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3.
Statistics
The percentage data were transformed into arcsine values to calculate the standard error (SE) of the mean. Differences between the means were analyzed using the Mann-Whitney U test at a 5% level of significance.
Mino M et al. (2005) Plant Cell Rep 24:179–188.
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Mino, M., Tezuka, T. & Shomura, S. The hybrid lethality of interspecific F1 hybrids of Nicotiana: a clue to understanding hybrid inviability—a major obstacle to wide hybridization and introgression breeding of plants. Mol Breeding 42, 10 (2022). https://doi.org/10.1007/s11032-022-01279-8
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DOI: https://doi.org/10.1007/s11032-022-01279-8
Keywords
- Plant breeding
- Wide hybridization
- Nicotiana species
- Hybrid inviability
- Plant immune system
- Chaperone complex