JIA-2021-2109 大麦分蘖生理与分子调控研究进展

doi:10.1016/j.jia.2022.08.011

摘要/Abstract

摘要： 分蘖是影响禾谷类作物产量潜力和环境适应性的一个重要性状，它既受内源（遗传）因子的控制，也受外源（环境）条件的影响。水稻与小麦分蘖的生理与分子调控已有大量研究，但相应的研究大麦上仍较少报导。作者在本综述中基于近年来生物信息学的研究成果将所有已知的大麦分蘖相关基因全部绘制在染色体物理图谱上，其中一些为首次在染色体上定位。本文还从遗传、生理和环境层面上讨论了分蘖的调控机理，构建了激素与糖代谢调控分蘖的遗传网络。同时，还阐述了环境因子与种植制度影响分蘖发生的原因。本综述可加深对大麦分蘖与相关发育特性生理与遗传调控机制的理解。

Abstract: Tillering is a crucial trait closely associated with yield potential and environmental adaptation in cereal crops, regulated by the synergy of endogenous (genetic) and exogenous (environmental) factors. The physiological and molecular regulation of tillering has been intensively studied in rice and wheat. However, tillering research on barley is scarce. This review used the recent advances in bioinformatics to map all known and potential barley tiller development genes with their chromosomal genetic and physical positions. Many of them were mapped for the first time. We also discussed tillering regulation at genetic, physiological, and environmental levels. Moreover, we established a novel link between the genetic control of phytohormones and sugars with tillering. We provided evidence of how environmental cues and cropping systems help optimize the tiller number. This comprehensive review enhances the understanding of barley’s physiological and genetic mechanisms controlling tillering and other developmental traits.

Key words: barley , development , genetic regulation , phytohormone , tillering

. JIA-2021-2109 大麦分蘖生理与分子调控研究进展[J]. Journal of Integrative Agriculture, 2023, 22(1): 1-13.

Asad RIAZ, Ahmad M. ALQUDAH, Farah KANWAL, Klaus PILLEN, YE Ling-zhen, DAI Fei, ZHANG Guo-ping. Advances in studies on the physiological and molecular regulation of barley tillering[J]. Journal of Integrative Agriculture, 2023, 22(1): 1-13.

参考文献

Abeledo L G, Calderini D F, Slafer G A. 2004. Leaf appearance, tillering and their coordination in old and modern barleys from argentina. Field Crops Research, 86, 23–32.
Agharkar M, Lomba P, Altpeter F, Zhang H, Kenworthy K, Lange T. 2007. Stable expression of AtGA2ox1 in a low-input turfgrass (Paspalum notatume) reduces bioactive gibberellin levels and improves turf quality under field conditions. Plant Biotechnology Journal, 5, 791–801.
Agusti J, Greb T. 2013. Going with the wind-adaptive dynamics of plant secondary meristems. Mechanisms of Development, 130, 34–44.
Alqudah A M, Koppolu R, Wolde G M, Graner A, Schnurbusch T. 2016. The genetic architecture of barley plant stature. Frontiers in Genetics, 7, 117.
Arend M, Schnitzler J P, Ehlting B, Hänsch R, Lange T, Rennenberg H, Himmelbach A, Grill E, Fromm J. 2009. Expression of the Arabidopsis mutant abi1 gene alters abscisic acid sensitivity, stomatal development, and growth morphology in gray poplars. Plant Physiology, 151, 2110–2119.
Babb S, Muehlbauer G. 2003. Genetic and morphological characterization of the barley uniculm2 (cul2) mutant. Theoretical and Applied Genetics, 106, 846–857.
Bahmaniar M, Ranjbar G. 2007. Response of rice cultivars to rates of nitrogen and potassium application in field and pot conditions. Pakistan Journal of Biological Sciences, 10, 1430–1437.
Bakht J, Shafi M, Zubair M, Khan M A, Shah Z. 2010. Effect of foliar vs. soil application of nitrogen on yield and yield components of wheat varieties. Pakistan Journal of Botany, 42, 2737–2745.
Balwinder-Singh E H, Gaydon D, Eberbach P. 2016. Evaluation of the effects of mulch on optimum sowing date and irrigation management of zero till wheat in central Punjab, India using apsim. Field Crops Research, 197, 83.
Barbier F, Cao D, Fichtner F, Weiste C, Perez-Garcia M D, Caradeuc M, Le Gourrierec J, Sakr S, Beveridge C A. 2021. Hexokinase1 signalling promotes shoot branching and interacts with cytokinin and strigolactone pathways. New Phytologist, 231, 1088–1104.
Bennett T, Sieberer T, Willett B, Booker J, Luschnig C, Leyser O. 2006. The Arabidopsis max pathway controls shoot branching by regulating auxin transport. Current Biology, 16, 553–563.
Beveridge C A, Kyozuka J. 2010. New genes in the strigolactone-related shoot branching pathway. Current Opinion in Plant Biology, 13, 34–39.
Bilsborough G D, Runions A, Barkoulas M, Jenkins H W, Hasson A, Galinha C, Laufs P, Hay A, Prusinkiewicz P, Tsiantis M. 2011. Model for the regulation of Arabidopsis thaliana leaf margin development. Proceedings of the National Academy of Sciences of the United States of America, 108, 3424–3429.
Borràs G, Romagosa I, Van Eeuwijk F, Slafer G A. 2009. Genetic variability in duration of pre-heading phases and relationships with leaf appearance and tillering dynamics in a barley population. Field Crops Research, 113, 95–104.
Le Bris M, Michaux-Ferrière N, Jacob Y, Poupet A, Barthe P, Guigonis J M, Le Page-Degivry M T. 1999. Regulation of bud dormancy by manipulation of ABA in isolated buds of rosa hybrida cultured in vitro. Functional Plant Biology, 26, 273–281.
Campoli C, Shtaya M, Davis S J, Von Korff M. 2012. Expression conservation within the circadian clock of a monocot: Natural variation at barley ppd-h1 affects circadian expression of flowering time genes, but not clock orthologs. BMC Plant Biology, 12, 97.
Chatfield S P, Stirnberg P, Forde B G, Leyser O. 2000. The hormonal regulation of axillary bud growth in Arabidopsis. The Plant Journal, 24, 159–169.
Chaturvedi G, Aggarwal P, Singh A, Joshi M, Sinha S. 1981. Effect of irrigation on tillering in wheat, triticale and barley in a water-limited environment. Irrigation Science, 2, 225–235.
Dabbert T, Okagaki R J, Cho S, Boddu J, Muehlbauer G J. 2009. The genetics of barley low-tillering mutants: Absent lower laterals (als). Theoretical and Applied Genetics, 118, 1351–1360.
Dabbert T, Okagaki R J, Cho S, Heinen S, Boddu J, Muehlbauer G J. 2010. The genetics of barley low-tillering mutants: Low number of tillers-1 (lnt1). Theoretical and Applied Genetics, 121, 705–715.
Dockter C, Hansson M. 2015. Improving barley culm robustness for secured crop yield in a changing climate. Journal of Experimental Botany, 66, 3499–3509.
Doebley J F, Gaut B S, Smith B D. 2006. The molecular genetics of crop domestication. Cell, 127, 1309–1321.
Domagalska M A, Leyser O. 2011. Signal integration in the control of shoot branching. Nature Reviews Molecular Cell Biology, 12, 211.
Donald C T. 1968. The breeding of crop ideotypes. Euphytica, 17, 385–403.
Doust A N, Kellogg E A. 2006. Effect of genotype and environment on branching in weedy green millet (Setaria viridis) and domesticated foxtail millet (Setaria italica)(poaceae). Molecular Ecology, 15, 1335–1349.
Druka A, Franckowiak J, Lundqvist U, Bonar N, Alexander J, Houston K, Radovic S, Shahinnia F, Vendramin V, Morgante M. 2011. Genetic dissection of barley morphology and development. Plant Physiology, 155, 617–627.
Dyck J A, Matus-Cádiz M A, Hucl P, Talbert L, Hunt T, Dubuc J P, Nass H, Clayton G, Dobb J, Quick J. 2004. Agronomic performance of hard red spring wheat isolines sensitive and insensitive to photoperiod. Crop Science, 44, 1976–1981.
Ferguson B J, Beveridge C A. 2009. Roles for auxin, cytokinin, and strigolactone in regulating shoot branching. Plant Physiology, 149, 1929–1944.
Fichtner F, Barbier F, Annunziata M G, Feil R, Olas J, Mueller-Roeber B, Stitt M, Beveridge C A, Lunn J E. 2021. Regulation of shoot branching in Arabidopsis by trehalose 6-phosphate. New Phytologist, 229, 2135–2151.
Fichtner F, Lunn J E. 2021. The role of trehalose 6-phosphate (Tre6P) in plant metabolism and development. Annual Review of Plant Biology, 72, 737–760.
Forster B P, Franckowiak J D, Lundqvist U, Lyon J, Pitkethly I, Thomas W T. 2007. The barley phytomer. Annals of Botany, 100, 725–733.
Franckowiak J D, Lundqvist U. 2002. Current list of new and revised barley genetic stock descriptions. Barley Genetics Newsletter, 32, 47.
Gallavotti A, Yang Y, Schmidt R J, Jackson D. 2008. The relationship between auxin transport and maize branching. Plant Physiology, 147, 1913–1923.
Gallavotti A, Zhao Q, Kyozuka J, Meeley R B, Ritter M K, Doebley J F, Pe M E, Schmidt R J. 2004. The role of barren stalk1 in the architecture of maize. Nature, 432, 630.
Gomez-Roldan V, Fermas S, Brewer P B, Puech-Pagès V, Dun E A, Pillot J P, Letisse F, Matusova R, Danoun S, Portais J C. 2008. Strigolactone inhibition of shoot branching. Nature, 455, 189.
González-Grandío E, Poza-Carrión C, Sorzano C O S, Cubas P. 2013. Branched1 promotes axillary bud dormancy in response to shade in Arabidopsis. The Plant Cell, 25, 834–850.
Giunta F, De Vita P, Mastrangelo A M, Sanna G, Motzo R. 2018. Environmental and genetic variation for yield-related traits of durum wheat as affected by development. Frontiers in Plant Science, 9, 8.
Herzig P, Maurer A, Draba V, Sharma R, Draicchio F, Bull H, Milne L, Thomas W T, Flavell A J, Pillen K. 2018. Contrasting genetic regulation of plant development in wild barley grown in two european environments revealed by nested association mapping. Journal of Experimental Botany, 69, 1517–1531.
Holubová K, Hensel G, Vojta P, Tarkowski P, Bergougnoux V, Galuszka P. 2018. Modification of barley plant productivity through regulation of cytokinin content by reverse-genetics approaches. Frontiers in Plant Science, 9, 1676.
Hussien A, Tavakol E, Horner D S, Muñoz-Amatriaín M, Muehlbauer G J, Rossini L. 2014. Genetics of tillering in rice and barley. The Plant Genome, 7, 10–32.
Islam T, Sedgley R. 1981. Evidence for a ‘uniculm effect’ in spring wheat (Triticum aestivum l.) in a mediterranean environment. Euphytica, 30, 277–282.
Jabran K, Ullah E, Hussain M, Farooq M, Zaman U, Yaseen M, Chauhan B. 2015. Mulching improves water productivity, yield and quality of fine rice under water-saving rice production systems. Journal of Agronomy and Crop Science, 201, 389–400.
Jasinski S, Piazza P, Craft J, Hay A, Woolley L, Rieu I, Phillips A, Hedden P, Tsiantis M. 2005. Knox action in Arabidopsis is mediated by coordinate regulation of cytokinin and gibberellin activities. Current Biology, 15, 1560–1565.
Jiao Y, Wang Y, Xue D, Wang J, Yan M, Liu G, Dong G, Zeng D, Lu Z, Zhu X. 2010. Regulation of OsSPL14 by OsmiR156 defines ideal plant architecture in rice. Nature Genetics, 42, 541.
Jones H, Kirby E. 1977. Effects of manipulation of number of tillers and water supply on grain yield in barley. The Journal of Agricultural Science, 88, 391–397.
Jones M, Singh M. 2000. Long-term yield patterns in barley-based cropping systems in northern Syria. 2. The role of feed legumes. The Journal of Agricultural Science, 135, 237–249.
Kato K, Miura H, Sawada S. 2000. Mapping QTLs controlling grain yield and its components on chromosome 5A of wheat. Theoretical and Applied Genetics, 101, 1114–1121.
Kebrom T H, Chandler P M, Swain S M, King R W, Richards R A, Spielmeyer W. 2012. Inhibition of tiller bud outgrowth in the tin mutant of wheat is associated with precocious internode development. Plant Physiology, 160, 308–318.
Kebrom T H, Mullet J E. 2015. Photosynthetic leaf area modulates tiller bud outgrowth in sorghum. Plant, Cell & Environment, 38, 1471–1478.
Kebrom T H, Richards R A. 2013. Physiological perspectives of reduced tillering and stunting in the tiller inhibition (tin) mutant of wheat. Functional Plant Biology, 40, 977–985.
Kebrom T H, Spielmeyer W, Finnegan E J. 2013. Grasses provide new insights into regulation of shoot branching. Trends in Plant Science, 18, 41–48.
Kirby E, Appleyard M. 1987. Cereal Development Guide. 2nd ed. Arable Unit, National Agricultural Center, Stoneleigh. United Kingdom.
Kirby E, Faris D. 1972. The effect of plant density on tiller growth and morphology in barley. The Journal of Agricultural Science, 78, 281–288.
Kirby E M, Appleyard M. 1981. Cereal Development Guide. Stoneleigh, United Kingdom.
Koppolu R, Anwar N, Sakuma S, Tagiri A, Lundqvist U, Pourkheirandish M, Rutten T, Seiler C, Himmelbach A, Ariyadasa R, Youssef H M, Stein N, Sreenivasulu N, Komatsuda T, Schnurbusch T. 2013. Six-rowed spike4 (Vrs4) controls spikelet determinacy and row-type in barley. Proceedings of the National Academy of Sciences of the United States of America, 110, 13198–13203.
Von Korff M, Wang H, Léon J, Pillen K. 2006. AB-QTL analysis in spring barley: I. Detection of favourable exotic alleles for agronomic traits introgressed from wild barley (H. vulgare ssp. Spontaneum). Theoretical and Applied Genetics, 112, 1221–1231.
Liao Z, Yu H, Duan J, Yuan K, Yu C, Meng X, Kou L, Chen M, Jing Y, Liu G. 2019. Slr1 inhibits moc1 degradation to coordinate tiller number and plant height in rice. Nature Communications, 10, 2738.
Liller C B, Neuhaus R, Von Korff M, Koornneef M, Van Esse W. 2015. Mutations in barley row type genes have pleiotropic effects on shoot branching. PLoS ONE, 10, e0140246.
Liu H, Li T, Wang Y, Zheng J, Li H, Hao C, Zhang X. 2019. TaZIM-A1 negatively regulates flowering time in common wheat (Triticum aestivum L.). Journal of Integrative Plant Biology, 61, 359–376.
Liu R, Finlayson S A. 2019. Sorghum tiller bud growth is repressed by contact with the overlying leaf. Plant, Cell & Environment, 42, 2120–2132.
Lo S F, Yang S Y, Chen K T, Hsing Y I, Zeevaart J A, Chen L J, Yu S M. 2008. A novel class of gibberellin 2-oxidases control semidwarfism, tillering, and root development in rice. The Plant Cell, 20, 2603–2618.
Lunn J E, Delorge I, Figueroa C M, Van Dijck P, Stitt M. 2014. Trehalose metabolism in plants. The Plant Journal, 79, 544–567.
Marzec M, Gruszka D, Tylec P, Szarejko I. 2016. Identification and functional analysis of the hvd14 gene involved in strigolactone signaling in Hordeum vulgare. Physiologia Plantarum, 158, 341–355.
Mascher M, Jost M, Kuon J E, Himmelbach A, Aßfalg A, Beier S, Scholz U, Graner A, Stein N. 2014. Mapping-by-sequencing accelerates forward genetics in barley. Genome Biology, 15, 1–15.
Mcsteen P, Malcomber S, Skirpan A, Wu X, Kellogg E, Hake S. 2007. Barren inflorescence2 encodes a co-ortholog of the pinoid serine/threonine kinase and is required for organogenesis during inflorescence and vegetative development in maize. Plant Physiology, 144, 1000–1011.
Minakuchi K, Kameoka H, Yasuno N, Umehara M, Luo L, Kobayashi K, Hanada A, Ueno K, Asami T, Yamaguchi S. 2010. Fine culm1 (fc1) works downstream of strigolactones to inhibit the outgrowth of axillary buds in rice. Plant and Cell Physiology, 51, 1127–1135.
Miralles D, Richards R. 2000. Responses of leaf and tiller emergence and primordium initiation in wheat and barley to interchanged photoperiod. Annals of Botany, 85, 655–663.
Mitchell J, Rebetzke G, Chapman S, Fukai S. 2013. Evaluation of reduced-tillering (tin) wheat lines in managed, terminal water deficit environments. Journal of Experimental Botany, 64, 3439–3451.
Miura K, Ikeda M, Matsubara A, Song X J, Ito M, Asano K, Matsuoka M, Kitano H, Ashikari M. 2010. Osspl14 promotes panicle branching and higher grain productivity in rice. Nature Genetics, 42, 545.
Müller J, Wang Y, Franzen R, Santi L, Salamini F, Rohde W. 2001. In vitro interactions between barley TALE homeodomain proteins suggest a role for protein–protein associations in the regulation of Knox gene function. The Plant Journal, 27, 13–23.
Naruoka Y, Talbert L E, Lanning S P, Blake N K, Martin J M, Sherman J D. 2011. Identification of quantitative trait loci for productive tiller number and its relationship to agronomic traits in spring wheat. Theoretical and Applied Genetics, 123, 1043–1053.
Nawab K, Shah P, Arif M, Ullah A, Khan M, Mateen A, Rab A, Munsif F, Ali K. 2011. Effect of cropping patterns, farm yard manure, K and Zn on wheat growth and grain yield. Sarhad Journal of Agriculture, 27, 371–375.
Nikovics K, Blein T, Peaucelle A, Ishida T, Morin H, Aida M, Laufs P. 2006. The balance between the mir164a and cuc2 genes controls leaf margin serration in Arabidopsis. The Plant Cell, 18, 2929–2945.
Okagaki R J, Cho S, Kruger W M, Xu W W, Heinen S, Muehlbauer G J. 2013. The barley uniculm2 gene resides in a centromeric region and may be associated with signaling and stress responses. Functional & Integrative Genomics, 13, 33–41.
Okagaki R J, Haaning A, Bilgic H, Heinen S, Druka A, Bayer M, Waugh R, Muehlbauer G J. 2018. Eligulum - A regulates lateral branch and leaf development in barley. Plant Physiology, 176, 2750–2760.
Otteson B N, Mergoum M, Ransom J, Schatz B. 2008. Tiller contribution to spring wheat yield under varying seeding and nitrogen management. Agronomy Journal, 100, 406–413.
Patil S B, Barbier F F, Zhao J, Zafar S A, Uzair M, Sun Y, Fang J, Perez-Garcia M, Bertheloot J, Sakr S, Fichtner F, Chabikwa T G, Yuan S, Beveridge C A, Li X. 2021. Sucrose promotes D53 accumulation and tillering in rice. New Phytologist, 234, 122–136.
Petrášek J, Friml J. 2009. Auxin transport routes in plant development. Development, 136, 2675–2688.
Pospíšilová H, Jiskrova E, Vojta P, Mrizova K, Kokáš F, Čudejková M M, Bergougnoux V, Plíhal O, Klimešová J, Novák O. 2016. Transgenic barley overexpressing a cytokinin dehydrogenase gene shows greater tolerance to drought stress. New Biotechnology, 33, 692–705.
Raman S, Greb T, Peaucelle A, Blein T, Laufs P, Theres K. 2008. Interplay of mir164, cup-shaped cotyledon genes and lateral suppressor controls axillary meristem formation in Arabidopsis thaliana. The Plant Journal, 55, 65–76.
Ramsay L, Comadran J, Druka A, Marshall D F, Thomas W T, Macaulay M, Mackenzie K, Simpson C, Fuller J, Bonar N. 2011. Intermedium-c, a modifier of lateral spikelet fertility in barley, is an ortholog of the maize domestication gene teosinte branched 1. Nature Genetics, 43, 169.
Romina P, Abeledo L G, Miralles D J. 2014. Identifying the critical period for waterlogging on yield and its components in wheat and barley. Plant and Soil, 378, 265–277.
Ruan J, Zhou Y, Zhou M, Yan J, Khurshid M, Weng W, Cheng J, Zhang K. 2019. Jasmonic acid signaling pathway in plants. International Journal of Molecular Sciences, 20, 2479.
Ruan Y L. 2012. Signaling role of sucrose metabolism in development. Molecular Plant, 5, 763–765.
Sakakibara H. 2006. Cytokinins: Activity, biosynthesis, and translocation. Annual Reviews of Plant Biology, 57, 431–449.
Sakamoto T, Kobayashi M, Itoh H, Tagiri A, Kayano T, Tanaka H, Iwahori S, Matsuoka M. 2001. Expression of a gibberellin 2-oxidase gene around the shoot apex is related to phase transition in rice. Plant Physiology, 125, 1508–1516.
Sakamoto T, Sakakibara H, Kojima M, Yamamoto Y, Nagasaki H, Inukai Y, Sato Y, Matsuoka M. 2006. Ectopic expression of knotted1-like homeobox protein induces expression of cytokinin biosynthesis genes in rice. Plant Physiology, 142, 54–62.
Schmitz G, Theres K. 2005. Shoot and inflorescence branching. Current Opinion in Plant Biology, 8, 506–511.
Shaaf S, Bretani G, Biswas A, Fontana I M, Rossini L. 2019. Genetics of barley tiller and leaf development. Journal of Integrative Plant Biology, 61, 226–256.
Shinohara N, Taylor C, Leyser O. 2013. Strigolactone can promote or inhibit shoot branching by triggering rapid depletion of the auxin efflux protein pin1 from the plasma membrane. PLoS Biology, 11, e1001474.
Skinner R, Simmons S. 1993. Modulation of leaf elongation, tiller appearance and tiller senescence in spring barley by far-red light. Plant, Cell & Environment, 16, 555–562.
Skirpan A, Culler A H, Gallavotti A, Jackson D, Cohen J D, Mcsteen P. 2009. Barren inflorescence2 interaction with zmpin1a suggests a role in auxin transport during maize inflorescence development. Plant and Cell Physiology, 50, 652–657.
Skirpan A, Wu X, Mcsteen P. 2008. Genetic and physical interaction suggest that BARREN STALK1 is a target of BARREN INFLORESCENCE2 in maize inflorescence development. The Plant Journal, 55, 787–797.
Stagnari F, Maggio A, Galieni A, Pisante M. 2017. Multiple benefits of legumes for agriculture sustainability: An overview. Chemical and Biological Technologies in Agriculture, 4, 1–13.
Tanaka R, Nakano H. 2019. Barley yield response to nitrogen application under different weather conditions. Scientific Reports, 9, 1–12.
Tantikanjana T, Yong J W, Letham D S, Griffith M, Hussain M, Ljung K, Sandberg G, Sundaresan V. 2001. Control of axillary bud initiation and shoot architecture in Arabidopsis through the supershoot gene. Genes & Development, 15, 1577–1588.
Tavakol E, Okagaki R, Verderio G, Shariati V, Hussien A, Bilgic H, Scanlon M J, Todt N R, Close T J, Druka A. 2015. The barley uniculme4 gene encodes a blade-on-petiole-like protein that controls tillering and leaf patterning. Plant Physiology, 168, 164–174.
Tucker D. 1977. The effects of far-red light on lateral bud outgrowth in decapitated tomato plants and the associated changes in the levels of auxin and abscisic acid. Plant Science Letters, 8, 339–344.
Vroemen C W, Mordhorst A P, Albrecht C, Kwaaitaal M A, De Vries S C. 2003. The cup-shaped cotyledon3 gene is required for boundary and shoot meristem formation in arabidopsis. The Plant Cell, 15, 1563–1577.
Wang G, Schmalenbach I, Von Korff M, Léon J, Kilian B, Rode J, Pillen K. 2010. Association of barley photoperiod and vernalization genes with QTLs for flowering time and agronomic traits in a BC2DH population and a set of wild barley introgression lines. Theoretical and Applied Genetics, 120, 1559–1574.
Wang H, Chen W, Eggert K, Charnikhova T, Bouwmeester H, Schweizer P, Hajirezaei M R, Seiler C, Sreenivasulu N, Von Wirén N. 2018. Abscisic acid influences tillering by modulation of strigolactones in barley. Journal of Experimental Botany, 69, 3883–3898.
Wiegmann M, Maurer A, Pham A, March T J, Al-Abdallat A, Thomas W T, Bull H J, Shahid M, Eglinton J, Baum M. 2019. Barley yield formation under abiotic stress depends on the interplay between flowering time genes and environmental cues. Scientific Reports, 9, 1–16.
Woodward E, Marshall C. 1988. Effects of plant growth regulators and nutrient supply on tiller bud outgrowth in barley (Hordeum distichum l.). Annals of Botany, 61, 347–354.
Xie Q, Mayes S, Sparkes D L. 2016. Optimizing tiller production and survival for grain yield improvement in a bread wheat× spelt mapping population. Annals of Botany, 117, 51–66.
Xing Y, Zhang Q. 2010. Genetic and molecular bases of rice yield. Annual Review of Plant Biology, 61, 421–442.
Xu P, Zhao P X, Cai X T, Mao J L, Miao Z Q, Xiang C B. 2020. Integration of jasmonic acid and ethylene into auxin signaling in root development. Frontiers in Plant Science, 11, 271.
Yamaguchi S. 2008. Gibberellin metabolism and its regulation. Annual Reviews of Plant Biology, 59, 225–251.
Yang L, Shao H, Wu Q X, Yu J, Rang C F, Li L Q, Li X. 2013. QTLs mapping and epistasis analysis for the number of tillers and spike number per plant in wheat. Journal of Triticeae Crops, 33, 875–882.
Yao C, Finlayson S A. 2015. Abscisic acid is a general negative regulator of Arabidopsis axillary bud growth. Plant Physiology, 169, 611–626.
Ye L, Wang Y, Long L, Luo H, Shen Q, Broughton S, Wu D, Shu X, Dai F, Li C. 2019. A trypsin family protein gene controls tillering and leaf shape in barley. Plant Physiology, 181, 701–713.
Yoshida A, Ohmori Y, Kitano H, Taguchi-Shiobara F, Hirano H Y. 2012. Aberrant spikelet and panicle1, encoding a topless-related transcriptional co-repressor, is involved in the regulation of meristem fate in rice. The Plant Journal, 70, 327–339.
Zazimalová E, Murphy A, Yang H, Hoyerova K, Hosek P. 2010. Auxin transporter - Why so many? Cold Spring Harbor Perspectives in Biology, 3, A001552.
Zhang Q, Wang Z, Miao F, Wang G. 2017. Dryland maize yield and water-use efficiency responses to mulching and tillage practices. Agronomy Journal, 109, 1196–1209.
Zou J, Zhang S, Zhang W, Li G, Chen Z, Zhai W, Zhao X, Pan X, Xie Q, Zhu L. 2006. The rice high-tillering dwarf1 encoding an ortholog of arabidopsis max3 is required for negative regulation of the outgrowth of axillary buds. The Plant Journal, 48, 687–698.