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Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Utilisation of stored lipids during germination in dimorphic seeds of euhalophyte Suaeda salsa

Yuanqin Zhao A , Yanchun Ma A , Qiang Li A , Yang Yang A , Jianrong Guo A and Jie Song A B
+ Author Affiliations
- Author Affiliations

A Shandong Provincial Key Laboratory of Plant Stress, College of Life Science, Shandong Normal University, Jinan 250014, PR China.

B Corresponding author. Email: songjieever@163.com

Functional Plant Biology 45(10) 1009-1016 https://doi.org/10.1071/FP17309
Submitted: 5 November 2017  Accepted: 26 March 2018   Published: 24 April 2018

Abstract

Utilisation of stored lipids plays an important role in germination of oil seeds. In the present study, key enzyme activity (lipase, isocitrate lyase and malate synthase) in lipid utilisation was determined during germination in dimorphic seeds of euhalophyte Suaeda salsa (L.) Pall. The results revealed that the percentage of germination were highest in intertidal brown seeds, followed by inland brown seeds and then inland black seeds moistened with 0 and 300 mM NaCl during early seed germination. The same trend was found in the activity of three enzymes and soluble sugar content when seeds were moistened with 0 and 300 mM NaCl for 3 h. Salinity reduced the activity of three enzymes in inland brown and black seeds in the initial 3 h, except that salinity had no adverse effect on isocitrate lyase activity of brown seeds. Salinity had no adverse effect on three enzymes in inland brown and black seeds in the initial 30 h, except that it decreased malate synthase activity of black seeds. Salinity had no effect on three enzymes in intertidal brown seeds in the initial 3 h and 30 h. In conclusion, high activity of these enzymes in brown seeds may play an important role in utilisation of stored lipids during their rapid seed germination.

Additional keywords: dimorphic seeds, germination, glyoxylate cycle, lipase, lipids, Suaeda salsa.


References

Arenashuertero F, Arroyo A, Zhou L, Sheen J, León P (2000) Analysis of Arabidopsis glucose insensitive mutants, gin5 and gin6, reveals a central role of the plant hormone ABA in the regulation of plant vegetative development by sugar. Genes & Development 14, 2085–2096.

Arzani A (2008) Improving salinity tolerance in crop plants: a biotechnological view. In Vitro Cellular & Developmental Biology. Plant 44, 373–383.
Improving salinity tolerance in crop plants: a biotechnological view.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVyltbnE&md5=63ee24e515a22e349940d9a9297d35d9CAS |

Beevers H (1980) The role of the glyoxylate cycle. In ‘The biochemistry of plants. A comprehensive treatise. Vol. 4: Lipids: structure and function’. (Ed. PK Stumpf) pp. 117–130. (Academic Press: New York)

Chell RM, Sundaram TK, Wilkinson AE (1978) Isolation and characterization of isocitrate lyase from a thermophillic Bacillus sp. The Biochemical Journal 173, 165–177.
Isolation and characterization of isocitrate lyase from a thermophillic Bacillus sp.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1cXmtFSqsLg%3D&md5=dbc7a8f9a023ec3d8d191ef126783ca9CAS |

Chen M, Song J, Wang BS (2010) NaCl increases the activity of the plasma membrane H+-ATPase in C3 halophyte Suaeda salsa callus. Acta Physiologiae Plantarum 32, 27–36.
NaCl increases the activity of the plasma membrane H+-ATPase in C3 halophyte Suaeda salsa callus.Crossref | GoogleScholarGoogle Scholar |

Chen TS, Yuan F, Song J, Wang BS (2016) Nitric oxide participates in waterlogging tolerance through enhanced adventitious root formation in the euhalophyte Suaeda salsa. Functional Plant Biology 43, 244–253.
Nitric oxide participates in waterlogging tolerance through enhanced adventitious root formation in the euhalophyte Suaeda salsa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XivVekurc%3D&md5=c78a65e6a50491cc360dde7d6c733cadCAS |

Cornah JE, Germain V, Ward JL, Beale MH, Smith SM (2004) Lipid utilization, gluconeogenesis, and seedling growth in Arabidopsis mutants lacking the glyoxylate cycle enzyme malate synthase. Journal of Biological Chemistry 279, 42916–42923.
Lipid utilization, gluconeogenesis, and seedling growth in Arabidopsis mutants lacking the glyoxylate cycle enzyme malate synthase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXotVOgt74%3D&md5=10c0a6b1c89c492b873d20ba3e31ce85CAS |

Dave A, Hernández ML, He Z, Andriotis VM, Vaistij FE, Larson TR, Graham IA (2011) 12-Oxo-phytodienoic acid accumulation during seed development represses seed germination in Arabidopsis. The Plant Cell 23, 583–599.
12-Oxo-phytodienoic acid accumulation during seed development represses seed germination in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXkvVOrsro%3D&md5=b1e5d68fd81df028a383037e252229ddCAS |

Eastmond PJ (2006) Sugar-dependent1 encodes a patatin domain triacylglycerol lipase that initiates storage oil breakdown in germinating Arabidopsis seeds. The Plant Cell 18, 665–675.
Sugar-dependent1 encodes a patatin domain triacylglycerol lipase that initiates storage oil breakdown in germinating Arabidopsis seeds.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XisFahurw%3D&md5=f1c59b76387fe06ce66dd8f7c0f1e2d7CAS |

Eastmond PJ, Germain V, Lange PR, Bryce JH, Smith SM, Graham IA (2000) Postgerminative growth and lipid catabolism in oilseeds lacking the glyoxylate cycle. Proceedings of the National Academy of Sciences of the United States of America 97, 5669–5674.
Postgerminative growth and lipid catabolism in oilseeds lacking the glyoxylate cycle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjsVWmtr4%3D&md5=e29ecde5b7939d6ddeb02bbd97166674CAS |

Eraslan F, Inal A, Gunes A, Alpaslan M (2007) Impact of exogenous salicylic acid on the growth, antioxidant activity and physiology of carrot plants subjected to combined salinity and boron toxicity. Scientia Horticulturae 113, 120–128.
Impact of exogenous salicylic acid on the growth, antioxidant activity and physiology of carrot plants subjected to combined salinity and boron toxicity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXlsF2rsrc%3D&md5=4cc0dae5c8c30be783c43562ec0bdff6CAS |

Finkelstein R, Reeves W, Ariizumi T, Steber C (2008) Molecular aspects of seed dormancy. Annual Review of Plant Biology 59, 387–415.
Molecular aspects of seed dormancy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXntFaqsbw%3D&md5=df3f41fbf1e20201d98cc394fb9fbe9eCAS |

Flowers TJ, Colmer TD (2015) Plant salt tolerance: adaptations in halophytes. Annals of Botany 115, 327–331.
Plant salt tolerance: adaptations in halophytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2sXhvFChurbP&md5=f2de4c131e6b7c98efcb68fe5edc9ccbCAS |

Fuchs C, Hansen G (1994) Partial purification and some properties of Brassica napus lipase. Zeitschrift Für Naturforschung C 49, 293–301.

Graham IA (2008) Seed storage oil mobilization. Annual Review of Plant Biology 59, 115–142.
Seed storage oil mobilization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXntFaqsLw%3D&md5=4885a6ebf906f4d8c55182d95871e2b4CAS |

Gul B, Ansari R, Flowers TJ, Khan MA (2013) Germination strategies of halophyte seeds under salinity. Environmental and Experimental Botany 92, 4–18.
Germination strategies of halophyte seeds under salinity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtFSnsA%3D%3D&md5=452bf2bc1aaea95dc3662660199df3e6CAS |

Guo JR, Suo SS, Wang BS (2015) Sodium chloride improves seed vigour of the euhalophyte Suaeda salsa. Seed Science Research 25, 335–344.
Sodium chloride improves seed vigour of the euhalophyte Suaeda salsa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhsVahsL7I&md5=ca06f2fda1d2e5d0c22bd1b506b71139CAS |

Guo J, Li Y, Han G, Song J, Wang B (2018) NaCl markedly improved the reproductive capacity of the euhalophyte Suaeda salsa. Functional Plant Biology 45, 350–361.
NaCl markedly improved the reproductive capacity of the euhalophyte Suaeda salsa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC1cXit1ylt7w%3D&md5=699e19d6fc12c3f7d87952a2df144adbCAS |

Imbert E (2002) Ecological consequences and ontogeny of seed heteromorphism. Perspectives in Plant Ecology, Evolution and Systematics 5, 13–36.
Ecological consequences and ontogeny of seed heteromorphism.Crossref | GoogleScholarGoogle Scholar |

Kanai M, Nishimura M, Hayashi M (2010) A peroxisomal ABC transporter promotes seed germination by inducing pectin degradation under the control of ABI5. The Plant Journal 62, 936–947.
A peroxisomal ABC transporter promotes seed germination by inducing pectin degradation under the control of ABI5.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXovFejsr4%3D&md5=9dcaba8f8f4e02c886c9b199f847a501CAS |

Kelly AA, Quettier AL, Shaw E, Eastmond PJ (2011) Seed storage oil mobilization is important but not essential for germination or seedling establishment in Arabidopsis. Plant Physiology 157, 866–875.
Seed storage oil mobilization is important but not essential for germination or seedling establishment in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlagsr7N&md5=3210996dfff2fde5c573f3d96d6c6349CAS |

Kornberg HL, Beevers H (1957a) A mechanism of conversion of fat to carbohydrate in castor beans. Nature 180, 35–36.
A mechanism of conversion of fat to carbohydrate in castor beans.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaG1cXntlSiuw%3D%3D&md5=e0f858e12bfd471d996d6e228a49e589CAS |

Kornberg HL, Beevers H (1957b) The glyoxylate cycle as a stage in the conversion of fat to carbohydrate in castor beans. Biochimica et Biophysica Acta 26, 531–537.
The glyoxylate cycle as a stage in the conversion of fat to carbohydrate in castor beans.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaG1cXjtVOntA%3D%3D&md5=01d78a2af149f6ad5f580f1a5a78f131CAS |

Kubicka E, Grabska J, Jedrychowski L, Czyz B (2000) Changes of specific activity of lipase and lipoxygenase during germination of wheat and barley. International Journal of Food Sciences and Nutrition 51, 301–304.
Changes of specific activity of lipase and lipoxygenase during germination of wheat and barley.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXlvFaitbw%3D&md5=11dc634488b946c940952a814ad463deCAS |

Kucera B, Cohn MA, Leubner-Metzger G (2005) Plant hormone interactions during seed dormancy release and germination. Seed Science Research 15, 281–307.
Plant hormone interactions during seed dormancy release and germination.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhsFGrtr0%3D&md5=04b112f49de790a30f9e6eb553349bcbCAS |

Kunce CM, Doman D (1984) Ontogeny of glyoxysomes in maturing and germinated cotton seeds – a morphometric analysis. Planta 161, 156–164.
Ontogeny of glyoxysomes in maturing and germinated cotton seeds – a morphometric analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXkt1SltLw%3D&md5=67aeedac6ef526ca38e7b3f75d8cdf3cCAS |

Leonova S, Grimberg , Å , Marttila S, Styme S, Carlsson AS (2010) Mobilization of lipid reserves during germination of oat (Avena sativa L.), a cereal rich in endosperm oil. Journal of Experimental Botany 61, 3089–3099.
Mobilization of lipid reserves during germination of oat (Avena sativa L.), a cereal rich in endosperm oil.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXotVWksbg%3D&md5=bfc73c527dc57026c8fcdc0a65e13868CAS |

Li WQ, Liu XJ, Khan MA, Yamaguchi S (2005) The effect of plant growth regulators, nitric oxide, nitrite and light on the germination of dimorphic seeds of Suaeda salsa under saline conditions. Journal of Plant Research 118, 207–214.
The effect of plant growth regulators, nitric oxide, nitrite and light on the germination of dimorphic seeds of Suaeda salsa under saline conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmt12qsL8%3D&md5=98a6b919f891ca729ce4c4723bdb51d6CAS |

Li X, Liu Y, Chen M, Song YP, Song J, Wang BS, Feng G (2012) Relationships between ion and chlorophyll accumulation in seeds and adaptation to saline environments in Suaeda salsa populations. Plant Biosystems 146, 142–149.
Relationships between ion and chlorophyll accumulation in seeds and adaptation to saline environments in Suaeda salsa populations.Crossref | GoogleScholarGoogle Scholar |

Lin YH, Wimer LT, Huang AHC (1983) Lipase in the lipid bodies of corn scutella during seedling growth. Plant Physiology 73, 460–463.
Lipase in the lipid bodies of corn scutella during seedling growth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXlvFWrtro%3D&md5=b9f8dbff8d5147cf322886de25155685CAS |

Liu QQ, Liu RR, Ma YC, Song J (2018) Physiological and molecular evidence for Na+ and Cl− exclusion in the roots of two Suaeda salsa populations. Aquatic Botany 146, 1–7.
Physiological and molecular evidence for Na+ and Cl exclusion in the roots of two Suaeda salsa populations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC1cXjvFKktw%3D%3D&md5=783ea6d090843c103236c9979c1c2317CAS |

Miransari M, Smith DL (2014) Plant hormones and seed germination. Environmental and Experimental Botany 99, 110–121.
Plant hormones and seed germination.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXislKjurw%3D&md5=6780d302a10956ee8d04cacdc75f5f65CAS |

Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annual Review of Plant Biology 59, 651–681.
Mechanisms of salinity tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXntFaqtrw%3D&md5=c43d04738daaecd46bd303bedcda90b3CAS |

Murphy DJ, Vance J (1999) Mechanisms of lipid-body formation. Trends in Biochemical Sciences 24, 109–115.
Mechanisms of lipid-body formation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXkslSjtLk%3D&md5=1236cb3b9b1848edfd3171e8199c8fa9CAS |

Qi CH, Chen M, Song J, Wang BS (2009) Increase in aquaporin activity is involved in leaf succulence of the euhalophyte Suaeda salsa under salinity. Plant Science 176, 200–205.
Increase in aquaporin activity is involved in leaf succulence of the euhalophyte Suaeda salsa under salinity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsFagtbrL&md5=116cecef27c92f19f9c4945456a03453CAS |

Quettier AL, Eastmond PJ (2009) Storage oil hydrolysis during early seedling growth. Plant Physiology and Biochemistry 47, 485–490.
Storage oil hydrolysis during early seedling growth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXltFWlurg%3D&md5=7d22ad75855d75ea1add50de13ad90faCAS |

Rajeshwara AN, Prakash V (2010) Purification and characterization of lipase from rice (Oryza sativa L.) bran. Molecular Nutrition & Food Research 39, 406–418.

Rozema J, Flowers T (2008) Crops for a salinized world. Science 322, 1478–1480.
Crops for a salinized world.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsFSisr%2FM&md5=860df4d0b72f1b6791f095aab8a9d1a3CAS |

Rozema J, Schat H (2013) Salt tolerance of halophytes, research questions reviewed in the perspective of saline agriculture. Environmental and Experimental Botany 92, 83–95.
Salt tolerance of halophytes, research questions reviewed in the perspective of saline agriculture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXovVCgsLk%3D&md5=f1e5eb79707f8f12f62931b773d82169CAS |

Smith SM (2002) Does the glyoxylate cycle have an anaplerotic function in plants? Trends in Plant Science 7, 12–13.
Does the glyoxylate cycle have an anaplerotic function in plants?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XntlCktg%3D%3D&md5=c6c87606950387aab19727212e47a1e8CAS |

Song J, Wang BS (2015) Using euhalophytes to understand salt tolerance and to develop saline agriculture: Suaeda salsa as a promising model. Annals of Botany 115, 541–553.
Using euhalophytes to understand salt tolerance and to develop saline agriculture: Suaeda salsa as a promising model.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2sXhvFChurjE&md5=a2165d6f15f94fa60b684f4c81cff193CAS |

Song J, Fan H, Zhao YY, Jia YH, Du XH, Wang BS (2008) Effect of salinity on germination, seedling emergence, seedling growth and ion accumulation of a euhalophyte Suaeda salsa, in an intertidal zone and on saline inland. Aquatic Botany 88, 331–337.
Effect of salinity on germination, seedling emergence, seedling growth and ion accumulation of a euhalophyte Suaeda salsa, in an intertidal zone and on saline inland.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjtl2hsr0%3D&md5=5027c2c1cff88bea661718ff5711486cCAS |

Song J, Shi G, Xing S, Yin C, Fan H, Wang BS (2009) Ecophysiological responses of the euhalophyte Suaeda salsa to the interactive effects of salinity and nitrate availability. Aquatic Botany 91, 311–317.
Ecophysiological responses of the euhalophyte Suaeda salsa to the interactive effects of salinity and nitrate availability.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFKntr3O&md5=21cb1873b6b19e5aedd8c6188685e970CAS |

Song J, Shi G, Gao B, Fan H, Wang B (2011) Waterlogging and salinity effects on two Suaeda salsa populations. Physiologia Plantarum 141, 343–351.
Waterlogging and salinity effects on two Suaeda salsa populations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXktlars7c%3D&md5=c02fae162354d006e7ac9ecaa84487e3CAS |

Song J, Shi WW, Liu RR, Xu YG, Sui N, Zhou JC, Feng G (2017) The role of the seed coat in adaptation of dimorphic seeds of the euhalophyte Suaeda salsa to salinity. Plant Species Biology 32, 107–114.
The role of the seed coat in adaptation of dimorphic seeds of the euhalophyte Suaeda salsa to salinity.Crossref | GoogleScholarGoogle Scholar |

Sui N, Tian SS, Wenqing WQ, Wang ML, Fan H (2017) Overexpression of glycerol-3-phosphate acyltransferase from Suaeda salsa improves salt tolerance in Arabidopsis. Frontiers in Plant Science 8, 1337
Overexpression of glycerol-3-phosphate acyltransferase from Suaeda salsa improves salt tolerance in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |

Tavener RJA, Laidman DL (1972) The induction of lipase activity in the germinating wheat grain. Phytochemistry 11, 989–997.
The induction of lipase activity in the germinating wheat grain.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE38XktVWks7s%3D&md5=62457fee778bf85acaf1c4eacde8d338CAS |

Turley RB, Trelease RN (1987) Cottonseed malate synthase: biogenesis in maturing and germinated seeds. Plant Physiology 84, 1350–1356.
Cottonseed malate synthase: biogenesis in maturing and germinated seeds.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXmtFCqs7w%3D&md5=8c377c1d5c714eec3c0258d9dec13913CAS |

Vijayakumar KR, Gowda LR (2012) Temporal expression profiling of lipase during germination and rice caryopsis development. Plant Physiology and Biochemistry 57, 245–253.
Temporal expression profiling of lipase during germination and rice caryopsis development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtFaitb%2FM&md5=b1bb60ddc310ee26b4638080c0baa4e6CAS |

Wang L, Dong M, Huang ZY (2010) Review of research on seed heteromorphism and its ecological significance. Journal of Plant Ecology 34, 578–590.

Wang L, Zhao ZY, Zhang K, Tian CY (2012) Oil content and fatty acid composition of dimorphic seeds of desert halophyte Suaeda aralocaspica. African Journal of Agricultural Research 7, 1910–1914.

Wang FX, Xu YG, Wang S, Shi WW, Liu RR, Feng G, Song J (2015) Salinity affects production and salt tolerance of dimorphic seeds of Suaeda salsa. Plant Physiology and Biochemistry 95, 41–48.
Salinity affects production and salt tolerance of dimorphic seeds of Suaeda salsa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhtFOksbvF&md5=08262d7f5d2a177f10e36ccebe473be6CAS |

Wang FX, Yin CH, Song YP, Li Q, Tian CY, Song J (2017) Reproductive allocation and fruit-set pattern in the euhalophyte Suaeda salsa in controlled and field conditions. Plant Biosystems
Reproductive allocation and fruit-set pattern in the euhalophyte Suaeda salsa in controlled and field conditions.Crossref | GoogleScholarGoogle Scholar |

Wanner G, Vigil EL, Theimer RR (1982) Ontogeny of microbodies (glyoxysomes) in cotyledons of dark-grown watermelon (Citrullus vulgaris Schrad.) seedlings: ultrastructural evidence. Planta 156, 314–325.
Ontogeny of microbodies (glyoxysomes) in cotyledons of dark-grown watermelon (Citrullus vulgaris Schrad.) seedlings: ultrastructural evidence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXjtFGgtA%3D%3D&md5=579edcff24724f7bfacb31e895c48821CAS |

Weber DJ, Ansari R, Gul B, Khan MA (2007) Potential of halophytes as source of edible oil. Journal of Arid Environments 68, 315–321.
Potential of halophytes as source of edible oil.Crossref | GoogleScholarGoogle Scholar |

Wobus U, Weber H (1999) Sugars as signal molecules in plant seed development. Biological Chemistry 380, 937–944.
Sugars as signal molecules in plant seed development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXls1Kks7w%3D&md5=da488f9204d3eadf88f7edb2d731c8dfCAS |

Xu YG, Liu RR, Sui N, Shi WW, Wang L, Tian CY, Song J (2016) Changes in endogenous hormones and seed coat phenolics during seed storage of two Suaeda salsa populations. Australian Journal of Botany 64, 325–332.
Changes in endogenous hormones and seed coat phenolics during seed storage of two Suaeda salsa populations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhtFSru7bF&md5=b9dffbeb91ff9ba61bb15950236ebe57CAS |

Xu YG, Zhao YQ, Duan HM, Sui N, Yuan F, Song J (2017) Transcriptomic profiling of genes in matured dimorphic seeds of euhalophyte Suaeda salsa. BMC Genomics 18, 727
Transcriptomic profiling of genes in matured dimorphic seeds of euhalophyte Suaeda salsa.Crossref | GoogleScholarGoogle Scholar |

Yamamoto Y, Beevers H (1960) Malate synthetase in higher plants. Plant Physiology 35, 102–108.
Malate synthetase in higher plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF3cXotFeguw%3D%3D&md5=def051aafb7c6480b2fdbf41220f056cCAS |

Yang F, Baskin JM, Baskin CC, Yang XJ, Cao DC, Huang ZY (2015) Effects of germination time on seed morph ratio in a seed-dimorphic species and possible ecological significance. Annals of Botany 115, 137–145.
Effects of germination time on seed morph ratio in a seed-dimorphic species and possible ecological significance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2sXhsVOgtr3K&md5=c0ab9a74f28c4296b6d495bf56053302CAS |

Zhang ZQ (1985) Determination of the soluble sugars in plant materials. In ‘Experimental handbook for plant physiology’. pp. 134–138. (Shanghai Science and Technology Press: Shanghai, China) [in Chinese]

Zhou JC, Fu TT, Sui N, Guo JR, Feng G, Fan JL, Song J (2016) The role of salinity in seed maturation of the euhalophyte Suaeda salsa. Plant Biosystems 150, 83–90.
The role of salinity in seed maturation of the euhalophyte Suaeda salsa.Crossref | GoogleScholarGoogle Scholar |