BBM Transcription Factors and Its Application in Apomixis of Kentucky Bluegrass (Poa pratensis)
LI Yu-Zhu, MIAO Jia-Min, YU Jiang-DI, ZHANG Yun-Kun, WANG Jing-Chang, YUE Wei-Nan, ZHANG Jin-Qing, LIU Yan, SHI Shang-Li, MA Hui-Ling*
College of Pratacultural Science, Gansu Agricultural University / Key Laboratory of Grassland Ecosystem, Ministry of Education / Pratacultural Engineering Laboratory of Gansu province / Sino-U.S. Center for Grassland Ecosystem Sustainability, Lanzhou 730070, China
Abstract：BBM (BABY BOOM), transcription factors of the AP2/ERF family are key regulators of plant cell totipotency. The BBM gene acts as a marker gene for parthenogenesis and plays a significant role to create the artificail apomixis in rice (Oryza sativa). The main objective of this review is to present recent advances in biotechnology of the BBM gene, a update on the current status on genetic mechanism of apomixis of Kentucky bluegrass (Poa pratensis) and its application in apomixis, in an aim to provide insights into breeding new cultivars and shortening the process of seed domestic production of Kentucky bluegrass via apomixis.
[1] 侯艳红, 龚桂芝, 彭祝春, 等. 2020. MIME-有丝分裂替代减数分裂及其在作物无融合生殖中的应用[J]. 生物工程学报, 36(3): 612-621. (Hou Y H, Gong G Z, Peng Z C, et al.2020. MIME-mitosis instead of meiosis and its application in crop apomixis[J]. Chinese Journal of Biotechnology, 36(3): 612-621.) [2] 黄大燊. 1997. 甘肃植被[M]. 甘肃科学技术出版社, 兰州. pp. 1-15. (Huang D S.1997. Vegetation of Gansu[M]. Gansu Science and Technology Press, Lanzhou. pp. 1-15.) [3] 黄群策. 1999. 禾本科植物无融合生殖的研究进展[J].武汉植物学研究, 17(增刊): 39-44. (Huang Q C.1999. Progress of XXXpomixes in poaceae[J]. Journal of Wuhan Botanical Research, 17(S1): 39-44) [4] 雷和田, 赵云云, 王景林, 等. 2000. 雾灵山草地早熟禾多胚囊和多胚现象的研究[J]. 植物学通报, 17(3): 270-273. (Lei H T, Zhao Y Y, Wang J L, et al.2000. Research on multiple embryo sacs and polyembryony in Poa pratensis L. in Wu-Ling-Shan[J]. Chinese bulletin of botany, 17(3): 270-273.) [5] 李和平, 孙蒙祥, 蔡得田, 等. 1996. 草地早熟禾胚胎学研究Ⅲ. 多胚囊及多胚现象[J]. 武汉植物学研究, 14(1): 25-29. (Li H P, Sun M X, Cai D T, et al.1996. Embryology study on Kentucky bluegrassⅢ. Multiple embryo sacs and polyembryony[J]. Journal of Wuhan Botanical Research, 14(1): 25-29.) [6] 刘燕, 张金青, 牛奎举, 等. 2020. 甘肃野生草地早熟禾种质资源无融合生殖鉴定分析[J]. 草原与草坪, 40(3): 84-89. (Liu Y, Zhang J Q, Niu K J, et al.2020. Identification of apomictic characteristics of wild Kentucky bluegrass germplasm resources in Gansu[J]. Grassland and Turf, 40(3): 84-89.) [7] 孙吉雄, 韩烈保. 2015. 草坪学[M]. 中国农业出版社, 北京. pp. 74-75. (Sun J X, Han L B.2015. Turf Science[M]. China Agriculture Press, Beijing. pp. 74-75.) [8] 孙敬三, 刘永胜, 辛化伟. 1996. 被子植物的无融合生殖[J]. 植物学通报, 13(1): 1-8. (Sun J S, Liu Y S, Xin H W.1996. Apomixis in angiosperms[J]. Chinese Bulletin of Botany, 13(1): 1-8.) [9] 赵桂琴, 曹致中. 1997. 草地早熟禾无融合生殖的细胞学鉴定[J]. 草业学报, 6(4): 64-70. (Zhao G Q, Cao Z Z.1997. Cytological identification of apomixis in Poa pratensis[J]. Acta Prataculturae Sinica, 6(4): 64-70.) [10] Akiyama Y, Conner J A, Goel S, et al.2004. High-resolution physical mapping in Pennisetum squamulatum reveals extensive chromosomal heteromorphism of the genomic region associated with apomixis[J]. Plant Physiology, 134, 1733-1741. [11] Albertini E, Barcaccia G, Porceddu A, et al.2001. Genetic control of parthenogenesis in Poa pratensis L.: Results from a sexual x apomictic cross[C]. Proceedings of the XIX International Grassland Congress, 138-139. [12] Albertini E, Marconi G, Barcaccia G, et al.2004. Isolation of candidate genes for apomixis in Poa pratensis L[J]. Plant Molecular Biology, 56(6): 879-894. [13] Albertini E, Mareoni G, Reale L, et al.2005. SERK and APOSTART candidate genes for apomixis in Poa pratensis[J]. Plant Physiology, 138: 2185-2199. [14] Anderson S N, Johnson C S, Chesnut J, et al.2017. The zygotic transition is initiated in unicellular plant zygotes with asymmetric activation of parental genomes[J]. Developmental Cell, 43(3): 349-358. [15] Anton A M, Connor H E.1995. Floral biology and reproduction in Poa (Poeae: Gramineae)[J]. Australian Journal of Botany, 43(6): 577-599. [16] Bantin J, Matzk F, Dresselhaus T.2001. Tripsacum dactyloides (Poaceae): A natural model system to study parthenogenesis[J]. Sexual Plant Reproduction, 14(4): 219-226. [17] Barcaccia G, Albertini E.2013. Apomixis in plant reproduction: A novel perspective on an old dilemma[J]. Plant Reproduction, 26: 159-179. [18] Barcaccia G, Mazzucato A, Albertini E, et al.1998. Inheritance of parthenogenesis in Poa pratensis L. auxin test and AFLP linkage analyses support monogenic control[J]. Theoretical and Applied Genetics, 97: 74-82. [19] Boutilier K, Offringa R, Sharma V K, et al.2002. Ectopic expression of BABY BOOM triggers a conversion from vegetative to embryonic growth[J]. Plant Cell, 14(8) :1737-1749. [20] Bui L T, Pandzic D, Youngstrom C E, et al.2017. A fern AINTEGUMENTA gene mirrors BABY BOOM in promoting apogamy in Ceratopteris richardii[J]. Plant Journal, 90: 122-132. [21] Calzada J P V, Crane C F, Stelly D M.1996. Apomixis: The asexual revolution[J]. Science, 274(5291): 1322-1323. [22] Conner J A, Gunawan G, Ozias-Akins P.2013. Recombination within the apospory specific genomic region leads to the uncoupling of apomixis components in Cenchrus ciliaris[J]. Planta, 238(1): 51-63. [23] Conner J A, Mookkan M, Huo H, et al.2015. A parthenogenesis gene of apomict origin elicits embryo formation from unfertilized eggs in a sexual plant[J]. Proceedings of National Academy of Sciences of the USA, 112:11205-11210. [24] Conner J A, Podio M, Ozias-akins P.2017. Haploid embryo production in rice and maize induced by PsASGR-BBML transgenes[J]. Plant Reproduction, 30(1): 41-52. [25] Czapik R.2000. Apomixis in monocotyledons[M]. CSIRO, Melbourne, pp. 316-321. [26] Ebina M, Nakagawa H, Yamamoto T, et al.2005. Co-segregation of AFLP and RAPD markers to apospory in Guineagrass (Panicum maximum Jacq.)[J]. Grassland Science, 51(1): 71-78. [27] Florez S L, Erwin R L, Maximova S N, et al.2015. Enhanced somatic embryogenesis in Theobroma cacao using the homologous BABY BOOM transcription factor[J]. BMC Plant Biology, 15(1): 121. [28] Floyd S K, Bowman J L.2007. The ancestral developmental tool kit of land plants[J]. International Journal of Plant Sciences, 168, 1-35. [29] Galitski T, Saldanha A J, Styles C A.1999. Ploidy regulation of gene expression[J]. Science, 285(5425): 251-253. [30] Grazi F, Umaerus M, Akerberg E.1961. Oberservations on the mode of reproduction and the embryology of Poa pratensis[J]. Hereditas, 47:489-541. [31] Hand M L, Koltunow A M G.2014. The genetic control of apomixis: Asexual seed formation[J]. Genetics, 197(2): 441-450. [32] Heidmann I, de Lange B, Lambalk J, et al.2011. Efficient sweet pepper transformation mediated by the BABY BOOM transcription factor[J]. Plant Cell Reports, 30: 1107-1115. [33] Horstman A, Willemsen V, Boutilier K, et al.2014. AINTEGUMENTA-Like proteins: Hubs in a plethora of networks[J]. Trends in Plant Science, 19: 146-157. [34] Jha P, Kumar V.2018. BABY BOOM (BBM):A candidate transcription factor gene in plant biotechnology[J]. Biotechnology Letters, 40: 1467-1475. [35] Jofuku K D, den Boer B G, Van Montagu M, et al.1994. Control of Arabidopsis flower and seed development by the homeotic gene APETELA2[J]. The Plant Cell, 6(9): 1211-1225. [36] Khanday I, Skinner D, Yang B, et al.2019. A male-expressed rice embryogenic trigger redirected for asexual propagation through seeds[J]. Nature, 565(7737): 91-95. [37] Kim S, Soltis P S, Wall K, et al.2006. Phylogeny and domain evolution in the APETALA2-like gene family[J]. Molecular Biology and Evolution, 23: 107-120. [38] Kulinska-Lukaszek K, Tobojka M, Adamiok A, et al.2012. Expression of the BBM gene during somatic embryogenesis of Arabidopsis thaliana[J]. Biologia Plantarum, 56: 389-394. [39] Labombarda P, Busti A, Caceres M E, et al.2002. An AFLP marker tightly linked to apomixis reveals hemizygosity in a portion of the apomixis-controlling locus in Paspalum simplex[J]. Genome, 45: 513-519. [40] Liu C, Li X, Meng D, et al.2017. A 4-bp Insertion at ZmPLA1 encoding a putative phospholipase a generates haploid induction in Maize[J]. Molecular Plant, 10(3): 520-522. [41] Lowe K, Wu E, Wang N, et al.2016. Morphogenic regulators Baby boom and Wuschel improve monocot transformation[J]. Plant Cell, 28: 1998-2015. [42] Lutz K A, Martin C, Khairzada S, et al.2015. Steroid-inducible BABY BOOM system for development of fertile Arabidopsis thaliana plants after prolonged tissue culture[J]. Plant Cell Reports, 34: 1849-1856. [43] Marconi G, Aiello D, Kindiger B, et al.2020. The role of APOSTART in switching between sexuality and apomixis in Poa pratensis[J]. Genes, 11(8): 941. [44] Matzk F, Meister A, Schubert I.2000. An efficient screen for reproductive pathways using mature seeds of monocots and dicots[J]. The Plant Journal, 21: 97-108. [45] Matzk F, Prodanovic S, Bäumlein H, et al.2005. The inheritance of apomixis in Poa pratensis confirms a five locus model with differences in gene expressivity and penetrance[J]. The Plant Cell, 17: 13-24. [46] Mazzucato A, Falcinelli M, Veronesi F.1996. Evolution and adaptedness in a facultatively apomictic grass, Poa pratensis L[J]. Euphytica, 92: 13-19. [47] Mookan M, Nelson-Vasilchik K, Hague J, et al.2017. Selectable marker independent transformation of recalcitrant maize inbred B73 and sorghum P898012 mediated by morphogenic regulators BABY BOOM and WUSCHEL2[J]. Plant Cell Reports, 36: 1477-1491. [48] Müntzing A.1933. Apomictic and sexual formation in Poa[J]. Hereclitas, 17(2): 131-154. [49] Nakano T, Suzuki K, Fujimura T, et al.2006. Genome-wide analysis of the ERF gene family in Arabidopsis and rice[J]. Plant Physiology, 140, 411-432. [50] Noyes R D, Baker R, Mai B.2007. Mendelian segregation for two-factor apomixis in Erigeron annuus (Asteraceae)[J]. Heredity, 98: 92-98. [51] Noyes R.D, Wagner J D.2014. Dihaploidy yields diploid apomicts and parthenogens in Erigeron (Asteraceae)[J]. American Journal of Botany, 101: 865-874. [52] Ogawa D, Johnson S D, Henderson S T, et al.2013. Genetic separation of autonomous endosperm formation (AutE) from two other components of apomixis in Hieracium[J]. Plant Reproduction, 26: 113-123. [53] Ortiz J P A, Leblanc O, Rohr C, et al.2019. Small RNA-seq reveals novel regulatory components for apomixis in Paspalum notatum[J]. BMC Genomics, 20(1): 487. [54] Ouakfaoui S E, Schnell J, Abdeen A, et al.2010. Control of somatic embryogenesis and embryo development by AP2 transcription factors[J]. Plant Molecular Biology, 74: 313-326. [55] Ozias-akins P.2006. Apomixis: Developmental characteristics and genetics[J]. Critical Reviews in Plant Sciences, 25(2): 199-214. [56] Passarinho P, Ketelaar T, Xing M, et al.2008. BABY BOOM target genes provide diverse entry points into cell proliferation and cell growth pathways[J]. Plant Molecular Biology, 68: 225-237. [57] Peter D, Jos D.2002. Apomixis technology and the paradox of sex[J]. Trends in Plant Science, 5(2): 81-84. [58] Porceddu A, Albertini E, Barcaccia G, et al.2002. Linkage mapping in apomictic and sexual Kentucky bluegrass (Poa pratensis L.) genotypes using a two way pseudo-testcross strategy based on AFLP and SAMPL markers[J]. Theoretical and Applied Genetics, 104: 273-280. [59] Richards A J.2003. Apomixis in flowering plants: An overview[J]. Philosophical Transactions of the Royal Society B, 358(1434): 1085-1093. [60] Riechmann J L, Meyerowitz E M.1998. The AP2/EREBP family of plant transcription factors[J]. The Journal of Biological Chemistry, 379, 633-646. [61] Roche D, Chen Z B, Hanna W W, et al.2001. Non-Mendelian transmission of an apospory-specific genomic region in a reciprocal cross between sexual pearl millet (Pennisetum glaucum) and an apomictic F1 (P. glaucum×P. squamulatum)[J]. Sexual Plant Reproduction, 13(4): 217-223. [62] Rodriguezleal D, Viellecalzada J P.2012. Regulation of apomixis: Learning from sexual experience[J]. Current Opinion in Plant Biology, 15(5): 549-555. [63] Sakuma Y, Liu Q, Dubouzet J G, et al.2002. DNA-binding specificity of the ERF/AP2 domain of Arabidopsis DREBs, transcription factors involved in dehydration- and cold-inducible gene expression[J]. Biochemical and biophysical research communications, 290(3): 998-1009. [64] Shivani, Awasthi P, Sharma V, et al.2017. Genome-wide analysis of transcription factors during somatic embryogenesis in banana (Musa spp.) cv. Grand Naine[J]. PLoS ONE, 12: e0182242. [65] Silva A T, Barduche D, do Livramento K G, et al.2015. A putative BABY BOOM-like gene (CaBBM) is expressed in embryogenic calli and embryogenic cell suspension culture of Coffea arabica L.[J]. In Vitro Cellular & Developmental Biology-Plant, 51: 93-101. [66] Spillane C, Steimer A, Grossniklaus U.2001. Apomixis in agriculture: The quest for clonal seeds[J]. Sexual Plant Reproduction, 14(4): 179-187. [67] Srinivasan C, Liu Z, Heidmann I, et al.2007. Heterologous expression of the BABY BOOM AP2/ERF transcription factor enhances the regeneration capacity of tobacco (Nicotiana tabacum L.)[J]. Planta, 225: 341-351. [68] Szenejko M, Rogalski M.2015. Characterization of morphological traits and RAPD polymorphism in selected forms of Kentucky bluegrass (Poa pratensis L.)[J]. Biodiversity Research & Conservation, 37(1): 1-10. [69] Tas I C, van Dijk P J.1999. Crosses between sexual and apomictic dandelions (Taraxacum). I. The inheritance of apomixis[J]. Heredity, 83: 707-714. [70] van Dijk P J, van Baarlen P, de Jong J H.2003. The occurrence of phenotypically complementary apomixis-recombinants in crosses between sexual and apomictic dandelions (Taraxacum officinale)[J]. Sexual Plant Reproduction, 16: 71-76. [71] van Dijk P J, Tas I C, Falque Met al.1999. Crosses between sexual and apomictic dandelions (Taraxacum). II. The breakdown of apomixis[J]. Heredity 83: 715-721. [72] Vijverberg K, Ozias-Akins P, Eric Schranz M E.2019. Identifying and engineering genes for parthenogenesis in plants[J]. Frontiers in Plant Science, 10: 128. [73] Vijverberg K, van Dijk P J.2007. Apomixis: Evolution, Mechanisms and Perspectives[M]. ARG Ganther Verlag KG, Ruggell, pp. 137-158. [74] Wang C, Liu Q, Shen Y, et al.2019. Clonal seeds from hybrid rice by simultaneous genome engineering of meiosis and fertilization genes[J]. Nature Biotechnology, 37(3): 283-286. [75] Yamashita K, Nakazawa Y, Namai K, et al.2012. Modes of inheritance of two apomixis components, diplospory and parthenogenesis, in Chinese chive (Allium ramosum) revealed by analysis of the segregating population generated by back-crossing between amphimictic and apomictic diploids[J]. Breeding Science, 62: 160-169. [76] Yang H F, Kou Y P, Gao B, et al.2014. Identification and functional analysis of BABY BOOM genes from Rosa canina[J]. Biologia Plantarum, 58: 427-435. [77] Yao L, Zhang Y, Liu C, et al.2018. OsMATL mutation induces haploid seed formation in indica rice[J]. Nature Plants, 4(8): 530-533.
