Abstract
Main Conclusion
Stomatal density and guard cell length of 274 global core germplasms of rapeseed reveal that the stomatal morphological variation contributes to global ecological adaptation and diversification of Brassica napus.
Abstract
Stomata are microscopic structures of plants for the regulation of CO2 assimilation and transpiration. Stomatal morphology has changed substantially in the adaptation to the external environment during land plant evolution. Brassica napus is a major crop to produce oil, livestock feed and biofuel in the world. However, there are few studies on the regulatory genes controlling stomatal development and their interaction with environmental factors as well as the genetic mechanism of adaptive variation in B. napus. Here, we characterized stomatal density (SD) and guard cell length (GL) of 274 global core germplasms at seedling stage. It was found that among the significant phenotypic variation, European germplasms are mostly winter rapeseed with high stomatal density and small guard cell length. However, the germplasms from Asia (especially China) are semi-winter rapeseed, which is characterized by low stomatal density and large guard cell length. Through selective sweep analysis and homology comparison, we identified several candidate genes related to stomatal density and guard cell length, including Epidermal Patterning Factor2 (EPF2; BnaA09g23140D), Epidermal Patterning Factor Like4 (EPFL4; BnaC01g22890D) and Suppressor of LLP1 (SOL1 BnaC01g22810D). Haplotype and phylogenetic analysis showed that natural variation in EPF2, EPFL4 and SOL1 is closely associated with the winter, spring, and semi-winter rapeseed ecotypes. In summary, this study demonstrated for the first time the relation between stomatal phenotypic variation and ecological adaptation in rapeseed, which is useful for future molecular breeding of rapeseed in the context of evolution and domestication of key stomatal traits and global climate change.
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Data accessibility
Raw reads of the rapeseed accessions are deposited in the public database of National Center of Biotechnology Information under SRP155312 (https://www.ncbi.nlm.nih.gov/sra/SRP155312).
References
Abrash EB, Davies KA, Bergmann DC (2011) Generation of signaling specificity in Arabidopsis by spatially restricted buffering of ligand—receptor interactions. Plant Cell 23:2864–2879. https://doi.org/10.1105/tpc.111.086637
Babla M, Cai S, Chen Z et al (2019) Molecular evolution and interaction of membrane transport and photoreception in plants. Front Genet 10:956–956. https://doi.org/10.3389/fgene.2019.00956
Bakker J (1991) Effects of humidity on stomatal density and its relation to leaf conductance. Sci Hortic 48:205–212. https://doi.org/10.1016/0304-4238(91)90128-L
Beerling D, Chaloner W (1993) The impact of atmospheric CO2 and temperature change on stomatal density: observations from quercus robur lammas leaves. Ann Bot 71:231–235. https://doi.org/10.1006/anbo.1993.1029
Beerling DJ, Royer DL (2002) Reading a CO2 signal from fossil stomata. New Phytol 153:387–397. https://doi.org/10.1046/j.0028-646X.2001.00335.x
Beerling DJ, Osborne CP, Chaloner WG (2001) Evolution of leaf-form in land plants linked to atmospheric CO2 decline in the late palaeozoic era. Nature (lond) 410:352–354. https://doi.org/10.1038/35066546
Bergmann DC, Sack FD (2007) Stomatal development. Annu Rev Plant Biol 58:163–181. https://doi.org/10.1146/annurev.arplant.58.032806.104023
Berry JA, Beerling DJ, Franks PJ (2010) Stomata: key players in the earth system, past and present. Curr Opin Plant Biol 13:232–239. https://doi.org/10.1016/j.pbi.2010.04.013
Bertolino LT, Caine RS, Gray JE (2019) Impact of stomatal density and morphology on water-use efficiency in a changing world. Front Plant Sci 10:225–225. https://doi.org/10.3389/fpls.2019.00225
Blasini DE, Koepke DF, Battipaglia G et al (2021) Adaptive trait syndromes along multiple economic spectra define cold and warm adapted ecotypes in a widely distributed foundation tree species. J Ecol 109:1298–1318. https://doi.org/10.1111/1365-2745.13557
Buckley CR, Caine RS, Gray JE (2020) Pores for thought: can genetic manipulation of stomatal density protect future rice yields? Front Plant Sci 10:1783–1783. https://doi.org/10.3389/fpls.2019.01783
Burgh JVD, Visscher H, Dilcher DL, Kurshner WM (1993) Paleoatmospheric signatures in neogene fossil leaves. Science 260:1788–1790. https://doi.org/10.1126/science.260.5115.1788
Cai S, Papanatsiou M, Blatt MR, Chen Z (2017) Speedy grass stomata: emerging molecular and evolutionary features. Mol Plant 10:912–914. https://doi.org/10.1016/j.molp.2017.06.002
Cai S, Huang Y, Chen F, Chen Z et al (2021) Evolution of rapid blue-light response linked to explosive diversification of ferns in angiosperm forests. New Phytol 230:1201–1213. https://doi.org/10.1111/nph.17135
Caine RS, Yin X, Gray JE et al (2018) Rice with reduced stomatal density conserves water and has improved drought tolerance under future climate conditions. New Phytol 221:371–384. https://doi.org/10.1111/nph.15344
Caldera HIU, Costa De, Ranwala SMW et al (2017) Effects of elevated carbon dioxide on stomatal characteristics and carbon isotope ratio of Arabidopsis thaliana ecotypes originating from an altitudinal gradient. Physiol Plant 159(1):74–92. https://doi.org/10.1111/ppl.12486
Casson S, Gray JE (2008) Influence of environmental factors on stomatal development. New Phytol 178:9–23. https://doi.org/10.1111/j.1469-8137.2007.02351.x
Casson SA, Hetherington AM (2010) Environmental regulation of stomatal development. Curr Opin Plant Biol 13:90–95. https://doi.org/10.1016/j.pbi.2009.08.005
Chalhoub B, Denoeud F, Wincker P et al (2014) Early allopolyploid evolution in the post-neolithic Brassica napus oilseed genome. Science 345:950–953. https://doi.org/10.1126/science.1253435
Chater CCC, Oliver J, Casson S, Gray JE (2014) Putting the brakes on: abscisic acid as a central environmental regulator of stomatal development. New Phytol 202:376–391. https://doi.org/10.1111/nph.12713
Chater CCC, Caine RS, Fleming AJ, Gray JE (2017) Origins and evolution of stomatal development. Plant Physiol (bethesda) 174:624–638. https://doi.org/10.1104/pp.17.00183
Chen X, Truksa M, Weselake RJ et al (2011) Three homologous genes encoding sn-glycerol-3-phosphate acyltransferase 4 exhibit different expression patterns and functional divergence in Brassica napus. Plant Physiol (bethesda) 155:851–865. https://doi.org/10.1104/pp.110.169482
Chen Z, Chen G, Blatt MR (2017) Molecular evolution of grass stomata. Trends Plant Sci 22:124–139. https://doi.org/10.1016/j.tplants.2016.09.005
Cheng F, Sun R, Wang X et al (2016) Subgenome parallel selection is associated with morphotype diversification and convergent crop domestication in Brassica rapa and Brassica oleracea. Nat Genet 48:1218–1224. https://doi.org/10.1038/ng.3634
Clifford SC, Black CR, Azam-Ali SN et al (1995) The effect of elevated atmospheric CO2 and drought on stomatal frequency in groundnut (Arachis hypogaea (L.)). J Exp Bot 46:847–852. https://doi.org/10.1093/jxb/46.7.847
Dittberner H, Korte A, Meaux J et al (2018) Natural variation in stomata size contributes to the local adaptation of water-use efficiency in Arabidopsis thaliana. Mol Ecol 27:4052–4065. https://doi.org/10.1111/mec.14838
Doheny-Adams T, Hunt L, Franks PJ, Beerling DJ, Gray JE (2012) Genetic manipulation of stomatal density influences stomatal size, plant growth and tolerance to restricted water supply across a growth carbon dioxide gradient. Philos Trans R Soc B-Biol Sci 367:547–555. https://doi.org/10.1098/rstb.2011.0272
Drake PL, Froend RH, Franks PJ (2013) Smaller, faster stomata: scaling of stomatal size, rate of response, and stomatal conductance. J Exp Bot 64:495–505. https://doi.org/10.1093/jxb/ers347
Dutton C, Hõrak H, Gray JE et al (2019) Bacterial infection systemically suppresses stomatal density. Plant, Cell Environ 42:2411–2421. https://doi.org/10.1111/pce.13570
Engineer CB, Ghassemian M, Schroeder JI et al (2014) Carbonic anhydrases, EPF2 and a novel protease mediate CO2 control of stomatal development. Nature (london) 513:246–250. https://doi.org/10.1038/nature13452
Franks PJ, Beerling DJ (2009) CO2-forced evolution of plant gas exchange capacity and water-use efficiency over the phanerozoic. Geobiology 7:27–236. https://doi.org/10.1111/j.1472-4669.2009.00193.x
Franks PJ, Doheny-Adams WT, Britton-Harper ZJ, Gray JE (2015) Increasing water-use efficiency directly through genetic manipulation of stomatal density. New Phytol 207:188–195. https://doi.org/10.1111/nph.13347
Fraser LH, Greenall A, Carlyle C, Turkington R, Friedman CR (2008) Adaptive phenotypic plasticity of Pseudoroegneria spicata: response of stomatal density, leaf area and biomass to changes in water supply and increased temperature. Ann Bot 103:769–775. https://doi.org/10.1093/aob/mcn252
Gan Z, Wang, et al (2010) Stomatal clustering, a new marker for environmental perception and adaptation in terrestrial plants. Bot Stud 51:325–336
Gay AP, Hurd RG (1975) The influence of light on stomatal density in the tomato. New Phytol 75:37–46. https://doi.org/10.1111/j.1469-8137.1975.tb01368.x
Gray JE, Holroyd GH, Hetherington AM et al (2000) The HIC signalling pathway links CO2 perception to stomatal development. Nature (london) 408:713–716. https://doi.org/10.1038/35047071
Hara K, Yokoo T, Kakimoto T et al (2009) Epidermal cell density is autoregulated via a secretory peptide, Epidermal Patterning Factor 2 in Arabidopsis leaves. Plant Cell Physiol 50:1019–1031. https://doi.org/10.1093/pcp/pcp068
Hetherington AM, Woodward FI (2003) The role of stomata in sensing and driving environmental change. Nature 424:901–908. https://doi.org/10.1038/nature01843
Holland N, Richardson AD (2009) Stomatal length correlates with elevation of growth in four temperate species. J Sustain for 28:63–73. https://doi.org/10.1080/10549810802626142
Huang Y, Tao Z, Wang H et al (2014) BnEPFL6, an EPIDERMAL PATTERNING FACTOR-LIKE (EPFL) secreted peptide gene, is required for filament elongation in Brassica napus. Plant Mol Biol 85:505–517. https://doi.org/10.1007/s11103-014-0200-2
Hughes J, Hepworth C, Gray JE et al (2017) Reducing stomatal density in barley improves drought tolerance without impacting on yield. Plant Physiol (bethesda) 174:776–787. https://doi.org/10.1104/pp.16.01844
Hunt L, Gray JE (2009) The signaling peptide EPF2 controls asymmetric cell divisions during stomatal development. Curr Biol 19:864–869. https://doi.org/10.1016/j.cub.2009.03.069
Jordan GJ (2011) A critical framework for the assessment of biological palaeoproxies: predicting past climate and levels of atmospheric CO2 from fossil leaves. New Phytol 192:29–44. https://doi.org/10.1111/j.1469-8137.2011.03829.x
Jordan GJ, Carpenter RJ, Brodribb TJ et al (2020) Links between environment and stomatal size through evolutionary time in proteaceae. Proc R Soc b, Biol Sci 287:2019–2876. https://doi.org/10.1098/rspb.2019.2876
Kang C, Lian H, Wang F, Huang J, Yang H (2009) Cryptochromes, phytochromes, and COP1 regulate light-controlled stomatal development in Arabidopsis. Plant Cell 21:2624–2641. https://doi.org/10.1105/tpc.109.069765
Kardiman R, Ræbild A (2018) Relationship between stomatal density, size and speed of opening in Sumatran rainforest species. Tree Physiol 38:696–705. https://doi.org/10.1093/treephys/tpx149
Ke Y, Wu Y, Du H et al (2020) Genome-wide survey of the bHLH super gene family in Brassica napus. BMC Plant Biol 20:115–115. https://doi.org/10.1186/s12870-020-2315-8
Klermund C, Ranftl QL, Schwechheimer C et al (2016) LLM-domain B-GATA transcription factors promote stomatal development downstream of light signaling pathways in Arabidopsis thaliana hypocotyls. Plant Cell 28:646–660. https://doi.org/10.1105/tpc.15.00783
Koini MA, Alvey L, Franklin KA et al (2009) High temperature-mediated adaptations in plant architecture require the bHLH transcription factor PIF4. Curr Biol 19:408–413. https://doi.org/10.1016/j.cub.2009.01.046
Lampard GR, MacAlister CA, Bergmann DC (2008) Arabidopsis stomatal initiation is controlled by MAPK-mediated regulation of the bHLH SPEECHLESS. Science 322:1113–1116. https://doi.org/10.1126/science.1162263
Lau OS, Bergmann DC (2012) Stomatal development: a plant’s perspective on cell polarity, cell fate transitions and intercellular communication. Development (cambridge) 139:3683–3692. https://doi.org/10.1242/dev.080523
Lau OS, Song Z, Bergmann DC et al (2018) Direct control of SPEECHLESS by PIF4 in the high-temperature response of stomatal development. Curr Biol 28:1273-1280.e3. https://doi.org/10.1016/j.cub.2018.02.054
Lawson T, Blatt MR (2014) Stomatal size, speed, and responsiveness impact on photosynthesis and water use efficiency. Plant Physiol (bethesda) 164:1556–1570. https://doi.org/10.1104/pp.114.237107
Lawson T, McElwain JC (2016) Evolutionary trade-offs in stomatal spacing. New Phytol 210:1149–1151. https://doi.org/10.1111/nph.13972
Lawson T, Vialet-Chabrand S (2019) Speedy stomata, photosynthesis and plant water use efficiency. New Phytol 221:93–98. https://doi.org/10.1111/nph.15330
Laza MRC, Kondo M, Ideta O, Barlaan E, Imbe T (2009) Quantitative trait loci for stomatal density and size in lowland rice. Euphytica 172:149–158. https://doi.org/10.1007/s10681-009-0011-8
Lee JS, Hnilova M, Torii KU et al (2015) Competitive binding of antagonistic peptides fine-tunes stomatal patterning. Nature (london) 522:439–443. https://doi.org/10.1038/nature14561
Leff B, Ramankutty N, Foley JA (2004) Geographic distribution of major crops across the world. Glob Biogeochem Cycles 18:GB1009. https://doi.org/10.1029/2003GB002108
Li M, Tian S, Li R et al (2013) Genomic analyses identify distinct patterns of selection in domesticated pigs and Tibetan wild boars. Nat Genet 45:1431–1438. https://doi.org/10.1038/ng.2811
Limin AE, Fowler DB (1994) Relationship between guard cell length and cold hardiness in wheat. Can J Plant Sci 74:59–62. https://doi.org/10.4141/cjps94-011
Limin AE, Fowler DB (2001) Inheritance of cell size in wheat (Triticum aestivum L.) and its relationship to the vernalization loci. Theor Appl Genet 103:277–281. https://doi.org/10.1007/s00122-001-0550-4
Lin G, Zhang L, Han Z et al (2017) A receptor-like protein acts as a specificity switch for the regulation of stomatal development. Genes Dev 31:927–938
Long Y, Shi J, Meng J et al (2007) Flowering time quantitative trait loci analysis of oilseed brassica in multiple environments and genomewide alignment with Arabidopsis. Genetics (austin) 177:2433–2444. https://doi.org/10.1534/genetics.107.080705
Lucas JR, Nadeau JA, Sack FD (2006) Microtubule arrays and Arabidopsis stomatal development. J Exp Bot 57:71–79. https://doi.org/10.1093/jxb/erj017
McAusland L, Vialet-Chabrand S, Lawson T et al (2016) Effects of kinetics of light-induced stomatal responses on photosynthesis and water-use efficiency. New Phytol 211:1209–1220. https://doi.org/10.1111/nph.14000
McElwain JC, Steinthorsdottir M (2017) Paleoecology, ploidy, paleoatmospheric composition, and developmental biology: a review of the multiple uses of fossil stomata. Plant Physiol (bethesda) 174:650–664. https://doi.org/10.1104/pp.17.00204
Miao L, Li S, Zhang Y et al (2020) Future drought in the dry lands of Asia under the 1.5 and 2.0 °C warming scenarios. Earth’s Future. https://doi.org/10.1029/2019EF001337
Miyazawa S, Livingston NJ, Turpin DH (2006) Stomatal development in new leaves is related to the stomatal conductance of mature leaves in poplar (Populus trichocarpa × P. deltoides). J Exp Bot 57:373–380. https://doi.org/10.1093/jxb/eri278
Nadeau JA, Sack FD (2002) Stomatal development in arabidopsis. Arabidopsis Book 1:e0066–e0066. https://doi.org/10.1199/tab.0066
Nagaharu U (1935) Genome analysis in Brassica with special reference to the experimental formation of B. napus and peculiar mode of fertilization. Jpn J Bot 7:389–452
O’Carrigan A, Hinde E, Chen Z et al (2014) Effects of light irradiance on stomatal regulation and growth of tomato. Environ Exp Bot 98:65–73. https://doi.org/10.1016/j.envexpbot.2013.10.007
Oberbauer SF, Strain BR (1986) Effects of canopy position and irradiance on the leaf physiology and morphology of Pentaclethra macroloba (mimosaceae). Am J Bot 73:409–416. https://doi.org/10.1002/j.1537-2197.1986.tb12054.x
Peterson CA, Fetcher N, McGraw JB, Bennington CC (2012) Clinal variation in stomatal characteristics of an arctic sedge, Eriophorum vaginatum (cyperaceae). Am J Bot 99:1562–1571. https://doi.org/10.3732/ajb.1100508
Pillitteri LJ, Torii KU (2012) Mechanisms of stomatal development. Annu Rev Plant Biol 63:591–614. https://doi.org/10.1146/annurev-arplant-042811-105451
Qi X, Torii KU (2018) Hormonal and environmental signals guiding stomatal development. BMC Biol 16:21–21. https://doi.org/10.1186/s12915-018-0488-5
Qi X, Han S, Dang JH, Torii KU et al (2017) Autocrine regulation of stomatal differentiation potential by EPF1 and ERECTA-LIKE1 ligand-receptor signaling. Elife. https://doi.org/10.7554/eLife.24102
Raissig MT, Matos JL, Bergmann DC et al (2017) Mobile MUTE specifies subsidiary cells to build physiologically improved grass stomata. Science 355:1215–1218. https://doi.org/10.1126/science.aal3254
Raven JA (2002) Selection pressures on stomatal evolution. New Phytol 153:371–386. https://doi.org/10.1046/j.0028-646X.2001.00334.x
Raven JA (2014) Speedy small stomata. J Exp Bot 65:1415–1424. https://doi.org/10.1093/jxb/eru032
Sankarasubramanian J, Vishnu US, Gunasekaran P, Rajendhran J (2016) A genome-wide SNP-based phylogenetic analysis distinguishes different biovars of Brucella suis. Infect Genet Evol 41:213–217. https://doi.org/10.1016/j.meegid.2016.04.012
Schlüter U, Muschak M, Berger D, Altmann T (2003) Photosynthetic performance of an Arabidopsis mutant with elevated stomatal density (SDD1-1) under different light regimes. J Exp Bot 54:867–874. https://doi.org/10.1093/jxb/erg087
Schoch P, Zinsou C, Sibi M (1980) Dependence of the stomatal index on environmental factors during stomatal differentiation in leaves of Vigna sinensis L.: 1. EFFECT of LIGHT intensity. J Exp Bot 31:1211–1216. https://doi.org/10.1093/jxb/31.5.1211
Simmons AR, Davies KA, Wang W, Liu Z, Bergmann DC (2019) SOL1 and SOL2 regulate fate transition and cell divisions in the Arabidopsis stomatal lineage. Development (cambridge). https://doi.org/10.1242/dev.171066
Song J, Guan Z, Hu J et al (2020) Eight high-quality genomes reveal pan-genome architecture and ecotype differentiation of Brassica napus. Nat Plants 6:34–45. https://doi.org/10.1038/s41477-019-0577-7
Spinoni J, Vogt JV, Naumann G, Barbosa P, Dosio A (2018) Will drought events become more frequent and severe in Europe? Int J Climatol 38:1718–1736. https://doi.org/10.1002/joc.5291
Stevens J, Faralli M, Wall S, Stamford JD, Lawson T (2021) Chapter 2 stomatal responses to climate change. Photosynthesis, respiration, and climate change. Springer International Publishing, pp 17–47. https://doi.org/10.1007/978-3-030-64926-5_2
Sun Y, Yan F, Cui X, Liu F (2014) Plasticity in stomatal size and density of potato leaves under different irrigation and phosphorus regimes. J Plant Physiol 171:1248–1255. https://doi.org/10.1016/j.jplph.2014.06.002
Takahashi S, Monda K, Iba K et al (2015) Natural variation in stomatal responses to environmental changes among Arabidopsis thaliana ecotypes. PLoS ONE 10:e0117449–e0117449. https://doi.org/10.1371/journal.pone.0117449
Taylor SH, Franks PJ, Osborne CP et al (2012) Photosynthetic pathway and ecological adaptation explain stomatal trait diversity amongst grasses. New Phytol 193:387–396. https://doi.org/10.1111/j.1469-8137.2011.03935.x
Tian M, Yu G, He N, Hou J (2016) Leaf morphological and anatomical traits from tropical to temperate coniferous forests: mechanisms and influencing factors. Sci Rep 6:19703–19703. https://doi.org/10.1038/srep19703
Torii KU (2021) Stomatal development in the context of epidermal tissues. Ann Bot 128:137–148. https://doi.org/10.1093/aob/mcab052
Wang Y, Chen Z (2020) Does molecular and structural evolution shape the speedy grass stomata? Front Plant Sci 11:333–333. https://doi.org/10.3389/fpls.2020.00333
Wang Y, Chen X, Xiang C (2007) Stomatal density and bio-water saving. J Integr Plant Biol 49:1435–1444. https://doi.org/10.1111/j.1672-9072.2007.00554.x
Wang D, Wang Y, Wan J et al (2017) SGD1, a key enzyme in tocopherol biosynthesis, is essential for plant development and cold tolerance in rice. Plant Sci (limerick) 260:90–100. https://doi.org/10.1016/j.plantsci.2017.04.008
Wayne RK, vonHoldt BM, Novembre J et al (2010) Genome-wide SNP and haplotype analyses reveal a rich history underlying dog domestication. Nature (london) 464:898–902. https://doi.org/10.1038/nature08837
Westbrook AS, McAdam SAM (2021) Stomatal density and mechanics are critical for high productivity: insights from amphibious ferns. New Phytol 229:877–889. https://doi.org/10.1111/nph.16850
Willmer C, Fricker M (1995) Stomata, 2nd edn. Chapman and Hall Ltd
Wu D, Liang Z, Jiang L et al (2019) Whole-genome resequencing of a worldwide collection of rapeseed accessions reveals the genetic basis of ecotype divergence. Mol Plant 12:30–43. https://doi.org/10.1016/j.molp.2018.11.007
Xiong D, Flexas J (2020) From one side to two sides: the effects of stomatal distribution on photosynthesis. New Phytol 228:1754–1766. https://doi.org/10.1111/nph.16801
Xu Z, Zhou G (2008) Responses of leaf stomatal density to water status and its relationship with photosynthesis in a grass. J Exp Bot 59:3317–3325. https://doi.org/10.1093/jxb/ern185
Yang M, Yang Q, Fu T, Zhou Y (2011) Overexpression of the Brassica napus BnLAS gene in Arabidopsis affects plant development and increases drought tolerance. Plant Cell Rep 30:373–388. https://doi.org/10.1007/s00299-010-0940-7
Yoo CY, Pence HE, Mickelbart MV et al (2011) The Arabidopsis GTL1 transcription factor regulates water use efficiency and drought tolerance by modulating stomatal density via transrepression of SDD1. Plant Cell 22:4128–4141. https://doi.org/10.1105/tpc.110.078691
Zhao L, Sack FD (1999) Ultrastructure of stomatal development in Arabidopsis (Brassicaceae) leaves. Am J Bot 86:929–939. https://doi.org/10.2307/2656609
Zhao W, Sun Y, Kjelgren R, Liu X (2014) Response of stomatal density and bound gas exchange in leaves of maize to soil water deficit. Acta Physiol Plant 37:1. https://doi.org/10.1007/s11738-014-1704-8
Zheng L, Van Labeke M (2018) Effects of different irradiation levels of light quality on chrysanthemum. Sci Hortic 233:124–131. https://doi.org/10.1016/j.scienta.2018.01.033
Zhu M, Dai S, McClung S, Yan X, Chen S (2009) Functional differentiation of Brassica napus guard cells and mesophyll cells revealed by comparative proteomics. Mol Cell Proteom 8:752–766. https://doi.org/10.1074/mcp.M800343-MCP200
Zhu M, Zhu N, Chen S et al (2014) Thiol-based redox proteins in abscisic acid and methyl jasmonate signaling in Brassica napus guard cells. Plant J Cell Mol Biol 78:491–515. https://doi.org/10.1111/tpj.12490
Zhu M, Zhang T, Chen S et al (2017) Redox regulation of a guard cell SNF1-related protein kinase in Brassica napus, an oilseed crop. Biochem J 474:2585–2599. https://doi.org/10.1042/BCJ20170070
Zoulias N, Harrison EL, Casson SA, Gray JE (2018) Molecular control of stomatal development. Biochem J 475:441–454. https://doi.org/10.1042/BCJ20170413
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This project is funded by the Zhejiang Provincial Key Research (2021C02057). We thank Dr. Ulrike Lohwasser (Germany) for providing the materials of the rapeseed accessions.
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Chen, Y., Zhu, W., Yan, T. et al. Stomatal morphological variation contributes to global ecological adaptation and diversification of Brassica napus. Planta 256, 64 (2022). https://doi.org/10.1007/s00425-022-03982-4
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DOI: https://doi.org/10.1007/s00425-022-03982-4