Scientia Agricultura Sinica ›› 2022, Vol. 55 ›› Issue (6): 1047-1063.doi: 10.3864/j.issn.0578-1752.2022.06.001

• CROP GENETICS & BREEDING·GERMPLASM RESOURCES·MOLECULAR GENETICS • Previous Articles     Next Articles

Research Progress on the Physiology and Its Molecular Mechanism of Seed Desiccation Tolerance

SONG SongQuan1,2(),LIU Jun1(),TANG CuiFang3,CHENG HongYan2,WANG WeiQing2,ZHANG Qi1,ZHANG WenHu1,GAO JiaDong1   

  1. 1Agro-Biological Gene Research Center, Guangdong Academy of Agricultural Sciences/Guangdong Provincial Key Lab for Crop Germplasm Resources Preservation and Utilization, Guangzhou 510640
    2Institute of Botany, Chinese Academy of Sciences, Beijing 100093
    3Shenzhen Qianhai Guoken Earth Fund Management Co., Ltd, Guangzhou 510630
  • Received:2021-08-12 Accepted:2021-10-08 Online:2022-03-16 Published:2022-03-25
  • Contact: SongQuan SONG,Jun LIU E-mail:sqsong@ibcas.ac.cn;liujun@gdaas.cn

Abstract:

Dehydration tolerance (DT) is defined as the ability of an organism or tissue to survive the removal of all, or almost all the cellular water without irreversible damage. DT of seeds is an adaptive mechanism to ensure the survival and reproduction of plant species in the long-term evolution process, and plays a key role in the conservation of plant seeds and germplasm resources. However, the DT of seeds is a complex trait, and its molecular mechanism is not now largely understood. Therefore, in the present paper, the research progresses on the physiological and molecular mechanisms of seed DT were reviewed. It was found that the DT of orthodox seeds was gradually formed during development, and reached the peak at physiological maturity. Recalcitrant seeds do not undergo the development stage of maturity dehydration, and are very sensitive to dehydration throughout development. Mature orthodox seeds maintained their resistance to re-dehydration at the initial stage of imbibition. With the time course of germination, the DT decreased gradually, and finally lost completely. The DT of seeds and embryos can be re-established during the early stage of germination, and of different tissues is different. The DT of seeds and embryos was inversely correlated with the decrease in mitochondrial respiratory activity. Respiratory activity of recalcitrant axis mitochondria was higher than that of orthodox embryo ones. During dehydration, the H2O2 content, the production rate of superoxide anion radical (·O2-) and the content of thiobarbituric acid reactive substance in desiccation-tolerant embryos (axes) were significantly lower than those of desiccation-sensitive embryos (axes), while the reactive oxygen species scavenging system in desiccation-tolerant embryos (axes), including enzymatic and non-enzymatic activities, was significantly higher than that in desiccation-sensitive embryos (axes). During the maturation of seeds, the accumulation of late embryogenesis abundant (LEA) proteins, small heat shock proteins and non-reducing oligosaccharides is closely related to the formation of DT. The AFL subfamily of B3 transcription factors (including ABI3 (ABA INSENSITIVE 3), FUS3 (FUSCA3) and LEC2 (LEAFY COTYLEDON 2)) increase the DT of seeds and embryos by positively regulating the accumulation of storage materials and protective proteins. The level of DNA methylation increased significantly throughout seed development and then decreased gradually during seed germination. Compared with embryos during the early stage of development and seedlings, mature embryos had a higher level of genomic methylation. In seeds, the parallel ABA and DOG1 (DELAY OF GERMINATION 1) signaling pathways activate synthesis of raffinose family oligosaccharides, and expression of LEA and HSP (heat shock protein) genes, thus regulating the onset of DT and transit to dormancy. Finally, the scientific issues that require to be further studied in this field are proposed, including the re-establishment of their model research system by using seeds and their tissues with different DT. Germinability, DT and dormancy characteristics of seeds are initiated and completed during development, and the relationship among them is still now unclear. There are both core ABA signaling pathway and DOG1 signaling pathway in seeds, and they converge at the ABI3 or downstream of ABI3. Which pathway will response preferentially and how these two pathways coordinate during dehydration of seeds? This paper will provide a reference for comprehensively understanding of the physiology and molecular mechanism of seed DT, increasing the stress resistance and yield of plant crops, improving the storage conditions of the resource bank and long-term preserving plant seed (germplasm) resources.

Key words: antioxidant system, desiccation tolerance, genetic regulation, long-term conservation of germplasm resource, metabolic activity, protective substance

Fig. 1

The effect of B3 transcription factors during the maturation of seeds [11] FUS3 represses TTG1 (TRANSPARENT TESTA GLABRA 1) transcription factor (TF), which is a negative regulator of genes related to fatty acid and storage protein biosynthesis, and positively regulates WRI1 (WRINKLED 1), an inducer of fatty acid biosynthesis; thus, FUS3 indirectly positively affects the accumulation of storage materials. FUS3 also regulates ABI3 expression in the lateral parts of cotyledons. LEC2 regulates other B3 TFs-FUS3 and ABI3, preventing anthocyanin and chlorophyll accumulation and takes part in intensified fatty acid biosynthesis and storage by positive regulation of WRI1 and OLE1; LEC2 also positively regulates the expression of 2S and 12S storage proteins. ABI3 regulates expression of FUS3 in the embryo axis and cotyledons and indirectly takes part in the accumulation of heat shock protective proteins by positive regulation of HSFA9 TF; ABI3 is a master regulator of late embryogenesis abundant (LEA) protective proteins"

Fig. 2

Abscisic acid (ABA) and DOG1 (DELAY OF GERMINATION 1) signaling pathways in seeds [12] The key elements of DOG1 signaling are heme molecule and PP2Cs encoded by AHG1 and AHG3 genes. Triplex complexes of PCAR-ABA-PP2C and/or DOG1-HEME-PP2C block the binding of PP2C to SnRK2. The active SnRK2 phosphorylates ABI3 and ABI5 which bind to the promoters (Pro) of ABA-controlled genes. In seeds, the parallel ABA and DOG1 signaling pathways activate synthesis of raffinose family oligosaccharide (RFO), expression of LEA and HSP genes, thus regulating the onset of desiccation tolerance and transit to dormancy. PYB/PYL/PCAR, pyrabactin resistance (PYR)/PYR-like/regulatory component of abscisic acid receptor; AHG, ABA hypersensitive germination; PP2C, group A type 2C protein phosphatase; SnRK2, subclass III sucrose-nonfermenting related kinase"

[1] BEWLEY J D, BRADFORD K J, HILHORST H W M, NONOGAKI H. Seeds: Physiology of Development, Germination and Dormancy. 3rd ed. New York: Springer, 2013.
[2] BLACK M, BEWLEY J D, HALMER P. The Encyclopedia of Seed. Science, Technology and Uses. Oxfordshire: CAB International, 2006.
[3] LEPRINCE O, BUITINK J. Desiccation tolerance: From genomics to the field. Plant Science, 2010,179:554-564.
doi: 10.1016/j.plantsci.2010.02.011
[4] OLIVER M J, FARRAN T J M, HILHORST H W M, MUNDREE S, WILLIAMS B, BEWLEY J D. Desiccation tolerance: Avoiding cellular damage during drying and rehydration. Annual Review of Plant Biology, 2020,71:435-460.
doi: 10.1146/annurev-arplant-071219-105542
[5] SONG S Q, BERJAK P, PAMMENTER N. Desiccation sensitivity of Trichilia dregeana Sond. axes and antioxidant role of ascorbic acid. Acta Botanica Sinica, 2004,46:803-810.
[6] 傅家瑞, 宋松泉. 顽拗性种子生物学. 北京: 中国科学文化出版社, 2004.
FU J R, SONG S Q. Recalcitrant Seed Biology. Beijing: China Science and Culture Press, 2004. (in Chinese)
[7] PAMMENTER N W, BERJAK P. Physiology of desiccation-sensitive (recalcitrant) seeds and the implications for cryopreservation. International Journal of Plant Science, 2014,175:21-28.
doi: 10.1086/673302
[8] KAN J, SONG S Q. Effects of dehydration, chilling, light, phytohormones and nitric oxide on germination of Pistia stratiotes seeds. Seed Science and Technology, 2008,36:38-45.
doi: 10.15258/sst
[9] BERJAK P, PAMMENTER N W. Implications of the lack of desiccation tolerance in recalcitrant seeds. Frontiers in Plant Science, 2013,4:478.
[10] BERJAK P, PAMMENTER N W. Recalcitrant seeds//BENECH- ARNOLD R L, SNCHEZ R A, eds. Handbook of Seed Physiology: Applications to Agriculture. New York: Haworth Press, 2014: 305-345.
[11] KIJAK H, RATAJCZAK E. What do we know about the genetic basis of seed desiccation tolerance and longevity? International Journal of Molecular Science, 2020,21:3612.
doi: 10.3390/ijms21103612
[12] SMOLIKOVA G, LEONOVA T, VASHURINA N, FROLOV A, MEDVEDEV S. Desiccation tolerance as the basis of long-term seed viability. International Journal of Molecular Sciences, 2021,22:101.
doi: 10.3390/ijms22010101
[13] WANG W Q, WANG Y, SONG X J, ZHANG Q, CHENG H Y, LIU J, SONG S Q. Proteomic analysis of desiccation tolerance and its re-establishment in different embryo axis tissues of germinated pea seeds. Journal of Proteome Research, 2021,20:2352-2363.
doi: 10.1021/acs.jproteome.0c00860
[14] XU X, LEGAY S, SERGEANT K, ZORZAN S, LECLERCQ C C, CHARTON S, GIAROLA V, LIU X, CHALLABATHULA D, RENAUT J, HAUSMAN J F, BARTELS D, GUERRIERO E. Molecular insights into plant desiccation tolerance: Transcriptomics, proteomics and targeted metabolite profiling in Craterostigma plantagineum. The Plant Journal, 2021,107:377-398.
doi: 10.1111/tpj.v107.2
[15] WU J H, WANG W Q, SONG S Q, CHENG H Y. Reactive oxygen species scavenging enzymes and down-adjustment of metabolism level in mitochondria associated with desiccation-tolerance acquisition of maize embryo. Journal of Integrative Plant Biology, 2009,51:638-645.
doi: 10.1111/jipb.2009.51.issue-7
[16] WANG W Q, YE J Q, ROGOWSKA-WRZESINSKA A, WOJDYLA K, JENSEN O N, MØLLER I M, SONG S Q. Proteomic comparison between maturation drying and prematurely imposed drying of Zea mayz seeds reveals a potential role of maturation drying in preparing proteins for seed germination, seedling vigor, and pathogen resistance. Journal of Proteome Research, 2013,13:606-626.
doi: 10.1021/pr4007574
[17] HUANG H, MØLLER I M, SONG S Q. Proteomics of desiccation tolerance during development and germination of maize embryos. Journal of Proteomics, 2012,75:1247-1262.
doi: 10.1016/j.jprot.2011.10.036
[18] HUANG H, SONG S Q, WU X J. Response of Chinese wampee axes and maize embryos on dehydration at different rates. Journal of Integrative Plant Biology, 2009,51:67-74.
doi: 10.1111/jipb.2008.51.issue-1
[19] 宋松泉, BERJAK P, PAMMENTER N W. Temporal pattern of changes in desiccation tolerance during imbibition of Pisum sativum seeds. 云南植物研究, 2009,31:239-246.
doi: 10.3724/SP.J.1143.2009.08216
SONG S Q, BERJAK P, PAMMENTER N W. Temporal pattern of changes in desiccation tolerance during imbibition of Pisum sativum seeds. Acta Botanica Yunnanica, 2009,31:239-246. (in Chinese)
doi: 10.3724/SP.J.1143.2009.08216
[20] WANG W Q, CHENG H Y, MØLLER I M, SONG S Q. The role of recovery of mitochondrial structure and function in desiccation tolerance of pea seeds. Physiologia Plantarum, 2012,144:20-34.
doi: 10.1111/ppl.2012.144.issue-1
[21] SONG S Q, FU J R. Studies on desiccation sensitivity and peroxidation of membrane lipids in lychee (Litch chinensis Sonn.) seeds. Chinese Science Bulletin, 1992,37:1470-1473.
[22] CHENG H Y, SONG S Q. Possible involvement of reactive oxygen species scavenging enzymes in desiccation sensitivity of Antiaris toxicaria seeds and axes. Journal of Integrative Plant Biology, 2008,50:1549-1556.
doi: 10.1111/jipb.2008.50.issue-12
[23] 宋松泉, 傅家瑞. 黄皮种子脱水敏感性与脂质过氧化作用. 植物生理学报, 1997,25:163-168.
SONG S Q, FU J R. Desiccation-sensitivity and lipid peroxidation in Chinese wampee [Clausena lansium (Lour.) Skeels] seeds. Acta Phytophysiologica Sinica, 1997,25:163-168. (in Chinese)
[24] 王伟青, 程红焱, 刘树君, 宋松泉. 黄皮种子线粒体呼吸速率和活性氧清除酶对脱水的响应及其生态学意义. 植物生态学报, 2012,36:870-879.
doi: 10.3724/SP.J.1258.2012.00870
WANG W Q, CHENG H Y, LIU S J, SONG S Q. Response of respiratory rate and reactive oxygen species scavenging enzyme activity in seed mitochondria of Clausena lansium dehydration and its ecological significance. Chinese Journal Plant Ecology, 2012,36:870-879. (in Chinese)
doi: 10.3724/SP.J.1258.2012.00870
[25] OBROUCHEVA N V, SINKEVICH I A, LITYAGINA S V. Physiological aspects of seed recalcitrance: A case study on the tree Aesculus hippocastanum. Tree Physiology, 2016,36:1127-1150.
doi: 10.1093/treephys/tpw037
[26] SONG S Q, TIAN M H, KAN J, CHENG H Y. The response difference of mitochondria in recalcitrant Antiaris toxicaria axes and orthodox Zea mays embryos to dehydration injury. Journal of Integrative Plant Biology, 2009,51:646-653.
doi: 10.1111/jipb.2009.51.issue-7
[27] STAVRINIDES A K, DUSSERT S, COMBES M C, FOCK-BASTIDE I, SEVERAC D, MINIER J, BASTOS-SIQUEIRA A, DEMOLOMBE V, HEM S, LASHERMESW P, JOËT T. Seed comparative genomics in three coffee species identify desiccation tolerance mechanisms in intermediate seeds. Journal of Experimental Botany, 2020,71:1418-1433.
doi: 10.1093/jxb/erz508
[28] LEPRINCE O, BUITINK J, HOEKSTRA F A. Axes and cotyledons of recalcitrant seeds of Castanea sativa Mill. exhibit contrasting responses of respiration to drying in relation to desiccation sensitivity. Journal of Experimental Botany, 1999,50:1515-1524.
doi: 10.1093/jxb/50.338.1515
[29] MØLLER I M. Plant mitochondria and oxidative stress: Electron transport, NADPH turnover, and metabolism of reactive oxygen species. Annual Review of Plant Physiology and Plant Molecular Biology, 2001,52:561-591.
doi: 10.1146/arplant.2001.52.issue-1
[30] BAILLY C. The signalling role of ROS in the regulation of seed germination and dormancy. Biochemical Journal, 2019,476:3019-3032.
doi: 10.1042/BCJ20190159
[31] DEL RÍO L A. ROS and RNS in plant physiology: An overview. Journal of Experimental Botany, 2015,66:2827-2837.
doi: 10.1093/jxb/erv099
[32] MITTLER R. ROS are good. Trends in Plant Science, 2017,22:11-19.
doi: 10.1016/j.tplants.2016.08.002
[33] DEMIDCHIK V. Reactive oxygen species and their role in plant oxidative stress//SHABALA S, ed. Plant Stress Physiology. CABI: Wallingford, 2017.
[34] MULLINEAUX P M, BAKER N R. Oxidative stress: Antagonistic signaling for acclimation or cell death? Plant Physiology, 2010,154:521-525.
doi: 10.1104/pp.110.161406
[35] JEEVAN KUMAR S P, RAJENDRA P S, BANERJEE R, THAMMINENI C. Seed birth to death: Dual functions of reactive oxygen species in seed physiology. Annals of Botany-London, 2015,116:663-668.
doi: 10.1093/aob/mcv098
[36] SANO N, RAJJOU L, NORTH H M, DEBEAUJON I, MARION-POLL A, SEO M. Staying alive: Molecular aspects of seed longevity. Plant Cell and Physiology, 2016,57:660-674.
doi: 10.1093/pcp/pcv186
[37] COLVILLE L, KRANNER I. Desiccation tolerant plants as model systems to study redox regulation of protein thiols. Plant Growth Regulation, 2016,2:241-255.
[38] FOYER C H, NOCTOR G. Redox homeostasis and antioxidant signaling: A metabolic interface between stress perception and physiological responses. The Plant Cell, 2005,17:1866-1875.
doi: 10.1105/tpc.105.033589
[39] RATAJCZAK E, MAŁECKA A, CIERESZKO I, STASZAK A M. Mitochondria are important determinants of the aging of seeds. International Journal of Molecular Science, 2019,20:1568.
doi: 10.3390/ijms20071568
[40] CHEN D, LI Y, FANG T, SHI X, CHEN X. Specific roles of tocopherols and tocotrienols in seed longevity and germination tolerance to abiotic stress in transgenic rice. Plant Science, 2016,244:31-39.
doi: 10.1016/j.plantsci.2015.12.005
[41] KUREK K, PLITTA-MICHALAK B, RATAJCZAK E. Reactive oxygen species as potential drivers of the seed aging process. Plants, 2019,8:174.
doi: 10.3390/plants8060174
[42] KRANNER I, MINIBAYEVA F V, BECKETT R P, SEAL C E. What is stress? Concepts, definitions and applications in seed science. New Phytologist, 2010,188:655-673.
doi: 10.1111/nph.2010.188.issue-3
[43] ROACH T, NAGEL M, BÖRNER A, EBERLE C, KRANNER I. Changes in tocochromanol and glutathione reveal differences in the mechanisms of seed ageing under seed bank conditions and controlled deterioration in barley. Environmental and Experimental Botany, 2018,156:8-15.
doi: 10.1016/j.envexpbot.2018.08.027
[44] SHVACHKO N A, KHLESTKINA E K. Molecular genetic bases of seed resistance to oxidative stress during storage. Vavilov Journal Genetics and Breeding, 2020,24:451-458.
doi: 10.18699/VJ20.637
[45] LEPRINCE O, PELLIZZARO A, BERRIRI S, BUITINK J. Late seed maturation: Drying without dying. Journal of Experimental Botany, 2017,68:827-841.
[46] MARQUES A, BUIJS G, LIGTERINK W, HILHORST H. Evolutionary ecophysiology of seed desiccation sensitivity. Functional Plant Biology, 2018,45:1083.
doi: 10.1071/FP18022
[47] DURE L I I I, GALAU G A. Developmental biochemistry of cottonseed embryogenesis and germination: XIII. Regulation of the biosynthesis of the principal storage proteins. Plant Physiology, 1981,68:187-194.
doi: 10.1104/pp.68.1.187
[48] BATTAGLIA M, COVARRUBIAS A A. Late embryogenesis abundant (LEA) proteins in legumes. Frontiers in Plant Science, 2013,4:190.
[49] COSTA M C D, COOPER K, HILHORST H W M, FARRANT J M. Orthodox seeds and resurrection plants: Two of a kind? Plant Physiology, 2017,175:589-599.
doi: 10.1104/pp.17.00760
[50] AMARA I, ZAIDI I, MASMOUDI K, LUDEVID M D, PAGÈS M, GODAY A, BRINI F. Insights into late embryogenesis abundant (LEA) proteins in plants: From structure to the functions. American Journal of Plant Sciences, 2014,5:3440-3455.
doi: 10.4236/ajps.2014.522360
[51] CANDAT A, PASZKIEWICZ G, NEVEU M, GAUTIER R, LOGAN D C, AVELANGE-MACHEREL M H, MACHEREL D. The ubiquitous distribution of late embryogenesis abundant proteins across cell compartments in Arabidopsis offers tailored protection against abiotic stress. The Plant Cell, 2014,26:3148-3166.
doi: 10.1105/tpc.114.127316
[52] HUNDERTMARK M, HINCHA D K. LEA (late embryogenesis abundant) proteins and their encoding genes in Arabidopsis thaliana. BMC Genomics, 2008,9:118.
doi: 10.1186/1471-2164-9-118
[53] ARTUR M A S, ZHAO T, LIGTERINK W, SCHRANZ E, HILHORST H W M. Dissecting the genomic diversification of late embryogenesis abundant (LEA) protein gene families in plants. Genome Biology and Evolution, 2019,11:459-471.
doi: 10.1093/gbe/evy248
[54] CHEN C, ZABAD S, LIU H, WANG W, JEFFERY C. MoonProt 2.0: An expansion and update of the moonlighting proteins database. Nucleic Acids Research, 2018,46:D640-D644.
doi: 10.1093/nar/gkx1043
[55] JIN X, CAO D, WANG Z, MA L, TIAN K, LIU Y, GONG Z, ZHU X, JIANG C, LI Y. Genome-wide identification and expression analyses of the LEA protein gene family in tea plant reveal their involvement in seed development and abiotic stress responses. Scientific Reports, 2019,9:14123.
doi: 10.1038/s41598-019-50645-8
[56] OLVERA-CARRILLO Y, CAMPOS F, REYES J L, GARCIARRUBIO A, COVARRUBIAS A A. Functional analysis of the group 4 late embryogenesis abundant proteins reveals their relevance in the adaptive response during water deficit in Arabidopsis. Plant Physiology, 2010,154:373-390.
doi: 10.1104/pp.110.158964
[57] FARRANT J M, PAMMENTER N W, BERJAK P. Seed development in relation to desiccation tolerance: A comparison between desiccation-sensitive (recalcitrant) seeds of Avicennia marina and desiccation-tolerant types. Seed Science Research, 1993,3:1-13.
doi: 10.1017/S0960258500001513
[58] DELAHAIE J, HUNDERTMARK M, BOVE J, LEPRINCE O, ROGNIAUX H, BUITINK J. LEA polypeptide profiling of recalcitrant and orthodox legume seeds reveals ABI3-regulated LEA protein abundance linked to desiccation tolerance. Journal of Experimental Botany, 2013,64:4559-4573.
doi: 10.1093/jxb/ert274
[59] JIN X, LIU D, MA L, GONG Z, CAO D, LIU Y, LI Y, JIANG C. Transcriptome and expression profiling analysis of recalcitrant tea (Camellia sinensis L.) seeds sensitive to dehydration. International Journal of Genomics, 2018,2018:5963797.
[60] DUSSERT S, SERRET J, BASTOS-SIQUEIRA A, MORCILLO F, DÈCHAMP E, ROFIDAL V, LASHERMES P, ETIENNE H, JOËT T. Integrative analysis of the late maturation programme and desiccation tolerance mechanisms in intermediate coffee seeds. Journal of Experimental Botany, 2018,69:1583-1597.
doi: 10.1093/jxb/erx492
[61] KALEMBA E M, PUKACKA S. Possible role of LEA proteins and sHSPs in seed protection: A short review. Biology Letters, 2007,44:3-16.
[62] KAUR H, PETLA B P, KAMBLE N U, SINGH A, RAO V, SALVI P, GHOSH S, MAJEE M. Differentially expressed seed aging responsive heat shock protein OsHSP18.2 implicates in seed vigor, longevity and improves germination and seedling establishment under abiotic stress. Frontiers in Plant Science, 2015,6:713.
[63] NOVER L, BHARTI K, DÖRING P, MISHRA S K, GANGULI A, SCHARF K D. Arabidopsis and the heat stress transcription factor world: How many heat stress transcription factors do we need? Cell Stress and Chaperones, 2001,6:177.
doi: 10.1379/1466-1268(2001)006<0177:AATHST>2.0.CO;2
[64] NETO V G, BARBOSA R R, CAROSIO M G A, FERREIRA A G, FERNANDEZ L G, DE CASTRO R D, LIGTERINK W, HILHORST H, RIBERIRO P R. Sequence analysis of Ricinus communis small heat shock protein (sHSP) subfamily and its role in abiotic stress responses. Industrial Crops and Products, 2020,152:112541.
doi: 10.1016/j.indcrop.2020.112541
[65] DEKKERS B J W, HE H, HANSON J, WILLEMS L A J, JAMER D C L, CUEFF G, RAJJOU L, HILHORST H W M, BENTSINK L. The Arabidopsis DELAY OF GERMINATION 1 gene affects ABSCISIC ACID INSENSITIVE 5 (ABI5) expression and genetically interacts with ABI3 during Arabidopsis seed development. The Plant Journal, 2016,85:451-465.
doi: 10.1111/tpj.13118
[66] BAUD S, DUBREUCQ B, MIQUEL M, ROCHAT C, LEPINIEC L. Storage reserve accumulation in Arabidopsis: Metabolic and developmental control of seed filling. The Arabidopsis Book, 2008,6:e0113.
doi: 10.1199/tab.0113
[67] BUITINK J, LEPRINCE O. Intracellular glasses and seed survival in the dry state. Comptes Rendus Biologies, 2008,331:788-795.
doi: 10.1016/j.crvi.2008.08.002
[68] WALTERS C. Orthodoxy, recalcitrance and in-between: Describing variation in seed storage characteristics using threshold responses to water loss. Planta, 2015,242:397-406.
doi: 10.1007/s00425-015-2312-6
[69] GONZÁLEZ-MORALES S I, CHÁVEZ-MONTES R A, HAYANO- KANASHIRO C, ALEJO-JACUINDE G, RICO-CAMBRON T Y, DE FOLTER S, HERRERA-ESTRELLA L. Regulatory network analysis reveals novel regulators of seed desiccation tolerance in Arabidopsis thaliana. Proceedings of the National Academy of Sciences of the United Stated America, 2016,113:E5232-E5241.
[70] JING Y, LANG S, WANG D, XUE H, WANG X F. Functional characterization of galactinol synthase and raffinose synthase in desiccation tolerance acquisition in developing Arabidopsis seeds. Journal of Plant Physiology, 2018,230:109-121.
doi: 10.1016/j.jplph.2018.10.011
[71] HELL A F, KRETZSCHMAR F S, SIMÕES K, HEYER A G, BARBEDO C J, BRAGA M R, CENTENO D C. Metabolic changes on the acquisition of desiccation tolerance in seeds of the brazilian native tree Erythrina speciosa. Frontiers in Plant Science, 2019,10:1356.
doi: 10.3389/fpls.2019.01356
[72] PUKACKA S, RATAJCZAK E, KALEMBA E. Non-reducing sugar levels in beech (Fagus sylvatica) seeds as related to withstanding desiccation and storage. Journal of Plant Physiology, 2009,166:1381-1390.
doi: 10.1016/j.jplph.2009.02.013
[73] INGRAM J, CHANDLER J W, GALLAGHER L, SALAMINI F, BARTELS D. Analysis of cDNA clones encoding sucrose-phosphate synthase in relation to sugar interconversions associated with dehydration in the resurrection plant Craterostigma plantagineum Hochst. Plant Physiology, 1997,115:113-121.
doi: 10.1104/pp.115.1.113
[74] PETERS S, MUNDREE S G, THOMSON J A, FARRANT J M, KELLER F. Protection mechanisms in the resurrection plant Xerophyta viscosa (Baker): Both sucrose and raffinose family oligosaccharides (RFOs) accumulate in leaves in response to water deficit. Journal of Experimental Botany, 2007,58:1947-1956.
doi: 10.1093/jxb/erm056
[75] YOSHIDA T, MOGAMI J, YAMAGUCHI-SHINOZAKI K. ABA- dependent and ABA-independent signaling in response to osmotic stress in plants. Current Opinion in Plant Biology, 2014,21:133-139.
doi: 10.1016/j.pbi.2014.07.009
[76] LIU S, LÜ Z, LIU Y, LI L, ZHANG L. Network analysis of ABA-dependent and ABA- independent drought responsive genes in Arabidopsis thaliana. Genetics and Molecular Biology, 2018,41:624-637.
doi: 10.1590/1678-4685-gmb-2017-0229
[77] FATIHI A, BOULARD C, BOUYER D, BAUD S, DUBREUCQ B, LEPINIEC L. Deciphering and modifying LAFL transcriptional regulatory network in seed for improving yield and quality of storage compounds. Plant Science, 2016,250:198-204.
doi: 10.1016/j.plantsci.2016.06.013
[78] CARBONERO P, IGLESIAS-FERNÁNDEZ R, VICENTE- CARBAJOSA J. The AFL subfamily of B3 transcription factors: Evolution and function in angiosperm seeds. Journal of Experimental Botany, 2017,68:871-880.
[79] YAMASAKI K, KIGAWA T, SEKI M, SHINOZAKI K, YOKOYAMA S. DNA-binding domains of plant-specific transcription factors: Structure, function, and evolution. Trends in Plant Science, 2013,18:267-276.
doi: 10.1016/j.tplants.2012.09.001
[80] BRAYBROOK S A, STONE S L, PARK S, BUI A Q, LE B H, FISCHER R L, GOLDBERG R B, HARADA J J. Genes directly regulated by LEAFY COTYLEDON 2 provide insight into the control of embryo maturation and somatic embryogenesis. Proceedings of the National Academy of Sciences of the United Stated America, 2006,103:3468-3473.
[81] GRIMAULT A, GENDROT G, CHAIGNON S, GILARD F, TCHERKEZ G, THÈVENIN J, DUBREUCQ B, DEPÈGE-FARGEIK N, ROGOWSKY P M. Role of B3 domain transcription factors of the AFL family in maize kernel filling. Plant Science, 2015,236:116-125.
doi: 10.1016/j.plantsci.2015.03.021
[82] TO A, VALON C, SAVINO G, GUILLEMINOT J, DRVIC M, GIRAUDAT J, PARCY F. A network of local and redundant gene regulation governs Arabidopsis seed maturation. The Plant Cell, 2006,18:1642-1651.
doi: 10.1105/tpc.105.039925
[83] RIGHETTI K, VU J L, PELLETIER S, VU B L, GLAAB E, LALANNE D, PASHA A, PATEL R V, PROVART N J, VERDIER J, LEPRINCE O, BUITINKA J. Inference of longevity-related genes from a robust coexpression network of seed maturation identifies regulators linking seed storability to biotic defense-related pathways. The Plant Cell, 2015,27:2692-2708.
[84] BIES-ETHÈVE N, GAUBIER-COMELLA P, DEBURES A, LASSERRE E, JOBET E, RAYNAL M, COOKE R, DELSENY M. Inventory, evolution and expression profiling diversity of the LEA (late embryogenesis abundant) protein gene family in Arabidopsis thaliana. Plant Molecular Biology, 2008,67:107-124.
doi: 10.1007/s11103-008-9304-x
[85] CHEN K, LI G, BRESSAN R A, SONG C, ZHU J, ZHAO Y. Abscisic acid dynamics, signaling, and functions in plants. Journal of Integrative Plant Biology, 2020,62:25-54.
doi: 10.1111/jipb.v62.1
[86] JO L, PELLETIER J M, HARADA J J. Central role of the LEAFY COTYLEDON 1 transcription factor in seed development. Journal of Integrative Plant Biology, 2019,61:564-580.
doi: 10.1111/jipb.v61.5
[87] BAUD S, MENDOZA M S, TO A, HARSCOËT E, LEPINIEC L, DUBREUCQ B. WRINKLED1 specifies the regulatory action of LEAFY COTYLEDON 2 towards fatty acid metabolism during seed maturation in Arabidopsis. The Plant Journal, 2007,50:825-838.
doi: 10.1111/j.1365-313X.2007.03092.x
[88] CHE N, YANG Y, LI Y, WANG L, HUANG P, GAO Y, AN C. Efficient LEC2 activation of OLEOSIN expression requires two neighboring RY elements on its promoter. Science in China Series C-Life Sciences, 2009,52:854-863.
doi: 10.1007/s11427-009-0119-z
[89] BRAYBROOK S A, HARADA J J. LECs go crazy in embryo development. Trends in Plant Science, 2008,13:624-630.
doi: 10.1016/j.tplants.2008.09.008
[90] GRAEBER K, NAKABAYASHI K, MIATTON E, LEUBNER- METZGER G, SOPPE W J J. Molecular mechanisms of seed dormancy. Plant Cell and Environment, 2012,35:1769-1786.
doi: 10.1111/pce.2012.35.issue-10
[91] WANG F, PERRY S E. Identification of direct targets of fusca3, a key regulator of Arabidopsis seed development. Plant Physiology, 2013,161:1251-1264.
doi: 10.1104/pp.112.212282
[92] CHEN M, ZHANG B, LI C, KULAVEERASINGAM H, CHEW F T, YU H. TRANSPARENT TESTA GLABRA 1 regulates the accumulation of seed storage reserves in Arabidopsis. Plant Physiology, 2015,169:391-402.
doi: 10.1104/pp.15.00943
[93] YAMAMOTO A, KAGAYA Y, USUI H, HOBO T, TAKEDA S, HATTORI T. Diverse roles and mechanisms of gene regulation by the Arabidopsis seed maturation master regulator FUS3 revealed by microarray analysis. Plant Cell and Physiology, 2010,51:2031-2046.
doi: 10.1093/pcp/pcq162
[94] BERR A, SHEN W H. Molecular mechanisms in epigenetic regulation of plant growth and development//PUA E C, DAVEY M R, eds. Plant Developmental Biology Biotechnological Perspectives. Springer: Berlin/Heidelberg Press, 2010: 325-344.
[95] CABEJ N R. Epigenetic Principles of Evolution. Elsevier Inc.: Amsterdam, The Netherlands, 2019: 733-781.
[96] PLITTA-MICHALAK B P, NASKRET-BARCISZEWSKA M Z, KOTLARSKI S, TOMASZEWSKI D, TYLKOWSKI T, BARCISZEWSKI J, CHMIELARZ P, MICHALAK M. Changes in genomic 5-methylcytosine level mirror the response of orthodox (Acer platanoides L.) and recalcitrant (Acer pseudoplatanus L.) seeds to severe desiccation. Tree Physiology, 2018,38:617-629.
doi: 10.1093/treephys/tpx134
[97] LEBEDEVA M A, TVOROGOVA V E, TIKHODEYEV O N. Epigenetic mechanisms and their role in plant development. Russian Journal of Genetics, 2017,53:1057-1071.
doi: 10.1134/S1022795417090083
[98] BOUYER D, KRAMDI A, KASSAM M, HEESE M, SCHNITTGER A, ROUDIER F, COLOT V. DNA methylation dynamics during early plant life. Genome Biology, 2017,18:1-12.
doi: 10.1186/s13059-016-1139-1
[99] BARTELS A, HAN Q, NAIR P, STACEY L, GAYNIER H, MOSLEY M, HUANG Q, PEARSON J, HSIEH T F, AN Y Q, XIAO W. Dynamic DNA methylation in plant growth and development. International Journal of Molecular Science, 2018,19:2144.
doi: 10.3390/ijms19072144
[100] KAWAKATSU T, NERY J R, CASTANON R, ECKER J R. Dynamic DNA methylation reconfiguration during seed development and germination. Genome Biology, 2017,18:1-12.
doi: 10.1186/s13059-016-1139-1
[101] CHEN M, LIN J Y, HUR J, PELLETIER J M, BADEN R, PELLEGRINI M, HARADA J J, GOLDBERG R B. Seed genome hypomethylated regions are enriched in transcription factor genes. Proceedings of the National Academy of Sciences of the United States of America, 2018,115:E8315-E8322.
[102] AN Y Q C, GOETTEL W, HAN Q, BARTELS A, LIU Z, XIAO W. Dynamic changes of genome-wide DNA methylation during soybean seed development. Scientific Reports, 2017,7:1-14.
doi: 10.1038/s41598-016-0028-x
[103] MICHALAK M, BARCISZEWSKA M Z, BARCISZEWSKI J, PLITTA B P, CHMIELARZ P. Global changes in DNA methylation in seeds and seedlings of Pyrus communis after seed desiccation and storage. PLoS ONE, 2013,8:e70693.
doi: 10.1371/journal.pone.0070693
[104] LI Y, KUMAR S, QIAN W. Active DNA demethylation: Mechanism and role in plant development. Plant Cell Report, 2018,37:77-85.
doi: 10.1007/s00299-017-2215-z
[105] ZHU J K. Active DNA demethylation mediated by DNA glycosylases. Annual Review of Genetics, 2009,43:143-166.
doi: 10.1146/genet.2009.43.issue-1
[106] LIU R, LANG Z. The mechanism and function of active DNA demethylation in plants. Journal of Integrative Plant Biology, 2020,62:148-159.
doi: 10.1111/jipb.v62.1
[107] LEPINIEC L, DEVIC M, ROSCOE T J, BOUYER D, ZHOU D X, BOULARD C, BAUD S, DUBREUCQ B. Molecular and epigenetic regulations and functions of the LAFL transcriptional regulators that control seed development. Plant Reproduction, 2018,31:291-307.
doi: 10.1007/s00497-018-0337-2
[108] NONOGAKI H. Seed germination and dormancy: The classic story, new puzzles, and evolution. Journal of Integrative Plant Biology, 2019,61:541-563.
doi: 10.1111/jipb.v61.5
[109] SALL K, DEKKERS B J W, NONOGAKI M, KATSURAGAWA Y, KOYARI R, HENDRIX D, WILLEMS L A J, BENTSINK L, NONOGAKI H. DELAY OF GERMINATION 1-LIKE 4 acts as an inducer of seed reserve accumulation. The Plant Journal, 2019,100:7-19.
doi: 10.1111/tpj.v100.1
[110] SOPPE W J J, BENTSINK L. Seed dormancy back on track; its definition and regulation by DOG1. New Phytologist, 2020,228:816-819.
doi: 10.1111/nph.v228.3
[111] GUTIERREZ L, WUYTSWINKEL O V, CASTELAIN M, BELLINI C. Combined networks regulating seed maturation. Trends in Plant Science, 2007,12:294-300.
doi: 10.1016/j.tplants.2007.06.003
[112] NAKABAYASHI K, BARTSCH M, XIANG Y, MIATTON E, PELLENGAHR S, YANO R, SEO M, SOPPE W J J. The time required for dormancy release in Arabidopsis is determined by DELAY OF GERMINATION1 protein levels in freshly harvested seeds. The Plant Cell, 2012,24:2826-2838.
doi: 10.1105/tpc.112.100214
[113] CUTLER S R, RODRIGUEZ P L, FINKELSTEIN R R, ABRAMS S R. Abscisic acid: Emergence of a core signaling network. Annual Review of Plant Biology, 2010,61:651-679.
doi: 10.1146/arplant.2010.61.issue-1
[114] DEJONGHE W, OKAMOTO M, CUTLER S R. Small molecule probes of ABA biosynthesis and signaling. Plant Cell and Physiology, 2018,59:1490-1499.
doi: 10.1093/pcp/pcy126
[115] XU P, CAI W. Function of Brassica napus BnABI3 in Arabidopsis gs1, an allele of AtABI3, in seed development and stress response. Frontiers in Plant Science, 2019,10:67.
doi: 10.3389/fpls.2019.00067
[116] NISHIMURA N, TSUCHIYA W, MORESCO J J, HAYASHI Y, SATOH K, KAIWA N, IRISA T, KIOOSHITA T, SCHROEDER J I, YATES J R, HIRAYAMA T, YAMAZAKI T. Control of seed dormancy and germination by DOG1-AHG1 PP2C phosphatase complex via binding to heme. Nature Communications, 2018,9:2132.
doi: 10.1038/s41467-018-04437-9
[117] DEKKERS B J W, BENTSINK L. Regulation of seed dormancy by abscisic acid and delay of germination 1. Seed Science Research, 2015,25:82-98.
doi: 10.1017/S0960258514000415
[118] MAIA J, DEKKERS B J W, DOLLE M J, LIGTERINK W, HILHORST H W M. Abscisic acid (ABA) sensitivity regulates desiccation tolerance in germinated Arabidopsis seeds. New Phytologist, 2014,203:81-93.
doi: 10.1111/nph.2014.203.issue-1
[1] ZiHan FAN,YaYin LUO,HuaYe XIONG,YuWen ZHANG,FuRong KANG,YuHeng WANG,Jie WANG,XiaoJun SHI,YueQiang ZHANG. Effect of Nitrification on Ammonium Toxicity to Citrus in Acidic Soil [J]. Scientia Agricultura Sinica, 2022, 55(18): 3600-3612.
[2] YIN Fei,LI ZhenYu,SAMINA Shabbir,LIN QingSheng. Expression and Function Analysis of Cytochrome P450 Genes in Plutella xylostella with Different Chlorantraniliprole Resistance [J]. Scientia Agricultura Sinica, 2022, 55(13): 2562-2571.
[3] DAI Si-lan, HONG Yan. Molecular Breeding for Flower Colors Modification on Ornamental Plants Based on the Mechanism of Anthocyanins Biosynthesis and Coloration [J]. Scientia Agricultura Sinica, 2016, 49(3): 529-542.
[4] SONG Shi-jia, SUN Hong-chun, ZHANG Yong-jiang, LIU Lian-tao, BAI Zhi-ying, LI Cun-dong. The Physiological Characteristics of the Antioxidant System of Colored Cotton and the Effects of Cellulose Accumulation on Cotton Fiber Quality [J]. Scientia Agricultura Sinica, 2015, 48(19): 3811-3820.
[5] HUI Zhu-Mei, WANG Zhi-Zhen, HU Yong, DENG Min-Min, ZHANG Zhen-Wen. Effects of 24-Epibrassinolide on the Antioxidant System and Osmotic Adjustment Substance in Grape Seedlings (V. vinifera L.) Under Chilling Stress [J]. Scientia Agricultura Sinica, 2013, 46(5): 1005-1013.
[6] ZHAO Peng, ZHANG Yi-Ting, HAO Li-Zhen, PANG Jie, YANG Zhong-Ren, ZHANG Feng-Lan. Effects of Ultra-Dry Treatment on Vigor and Antioxidative Metabolism of Pugionium Seeds [J]. Scientia Agricultura Sinica, 2013, 46(2): 334-342.
[7] ZHANG Fan, YU Ji-Hua, JIE Jian-Ming, FENG Zhi, ZHANG Guo-Bin, LI Wen-Lin. Influence of Exogenous ALA and Spd on Photosynthesis and Antioxidant System of Low Temperature and Poor Light Affected Pepper Seedlings [J]. Scientia Agricultura Sinica, 2013, 46(11): 2298-2306.
[8] LI Yong-hong,MA Ying-min,XU Bai-qiu,ZHAO Liang-jun
. Relationship Between Dehydration Tolerance and Soluble Sugars During Seed Development of Pachira macrocarpa
[J]. Scientia Agricultura Sinica, 2009, 42(8): 2882-2891 .
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed   
No Suggested Reading articles found!