NaCl markedly improved the reproductive capacity of the euhalophyte Suaeda salsa
Jianrong Guo A , Yandi Li A , Guoliang Han A , Jie Song A and Baoshan Wang A BA Key Lab of Plant Stress Research, College of Life Sciences, Shandong Normal University, Ji’nan, Shandong, 250014, PR China.
B Corresponding author. Email: bswang@sdnu.edu.cn
Functional Plant Biology 45(3) 350-361 https://doi.org/10.1071/FP17181
Submitted: 27 June 2017 Accepted: 23 September 2017 Published: 16 October 2017
Abstract
The effect of NaCl on reproductive development was investigated in euhalophyte Suaeda salsa L. under controlled conditions. Results showed that NaCl promoted the reproductive growth of S. salsa and 200 mM NaCl was optimal. This was reflected in the increases of seed yield, seed number, flower number per plant and leaf axil, 1000 seed weight, as well as a decrease in flower abortion percentage with supply of NaCl. NaCl reduced the flower abortion percentage by increasing stigma receptivity instead of pollen viability. The Na+ and Cl– concentration in petals, stems and leaves were increased significantly but slightly in stamen and pistil. In contrast, the K+ concentration decreased markedly in leaves, stems and petals but a little in stamen and pistil. The Na+ and Cl– concentrations also increased significantly in seed from mother plants exposed to NaCl, whereas K+ decreased. However, seed quality was not influenced. Our results showed that high concentration of NaCl markedly increases the seed number and quality of S. salsa primarily via increasing flower number and fertility and S. salsa develops strategy to maintain ion homeostasis in reproductive organs for the generation. These factors play a pivotal role in setting up plant populations in saline environment.
Additional keywords: ion concentration, reproductive success, salt.
References
Abdullah Z, Khan MA, Flowers TJ (2001) Causes of sterility in seed set of rice under salinity stress. Journal Agronomy & Crop Science 187, 25–32.| Causes of sterility in seed set of rice under salinity stress.Crossref | GoogleScholarGoogle Scholar |
Alexander M (1969) Differential staining of aborted and nonaborted pollen. Stain Technology 44, 117–122.
| Differential staining of aborted and nonaborted pollen.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaF1M7ptlajug%3D%3D&md5=d6196602f88f87203147649722470185CAS |
Amzallag GN (2005) Perturbed reproductive development in salt treated Sorghum bicolor: a consequence of modifications in regulation network? Journal of Experimental Botany 56, 2821–2829.
| Perturbed reproductive development in salt treated Sorghum bicolor: a consequence of modifications in regulation network?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFCjt7vL&md5=643c0d27a33b658df2a1547748eae99dCAS |
Baby T, Collins C, Tyerman SD, Gilliham M (2016) Salinity negatively affects pollen tube growth and fruit set in grapevines and cannot be ameliorated by silicon. American Journal of Enology and Viticulture 67, 218–228.
| Salinity negatively affects pollen tube growth and fruit set in grapevines and cannot be ameliorated by silicon.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2sXmtVSltLg%3D&md5=a2a22b73f510b1bdb1f6b787b0e0758aCAS |
Bustan A, Pasternak D, Pirogova I, Durikov M, Devries TT, El-Meccawi S, Degen AA (2005) Evaluation of saltgrass as a fodder crop for livestock. Journal of the Science of Food and Agriculture 85, 2077–2084.
| Evaluation of saltgrass as a fodder crop for livestock.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXpvF2rtL4%3D&md5=93a880af1fff2f994b2afb8b16aa3013CAS |
Cheeseman JM (2015) The evolution of halophytes, glycophytes and crops, and its implications for food security under saline conditions. New Phytologist 206, 557–570.
| The evolution of halophytes, glycophytes and crops, and its implications for food security under saline conditions.Crossref | GoogleScholarGoogle Scholar |
Davy AJ, Bishop GF, Costa CSB (2001) Salicornia L.(Salicornia pusilla J. Woods, S. ramosissima J. Woods, S. europaea L., S. obscura PW Ball & Tutin, S. nitens PW Ball & Tutin, S. fragilis PW Ball & Tutin and S. dolichostachya Moss). Journal of Ecology 89, 681–707.
| Salicornia L.(Salicornia pusilla J. Woods, S. ramosissima J. Woods, S. europaea L., S. obscura PW Ball & Tutin, S. nitens PW Ball & Tutin, S. fragilis PW Ball & Tutin and S. dolichostachya Moss).Crossref | GoogleScholarGoogle Scholar |
Debez A, Hamed KB, Grignon C, Abdelly C (2004) Salinity effects on germination, growth, and seed production of the halophyte Cakile maritima. Plant and Soil 262, 179–189.
| Salinity effects on germination, growth, and seed production of the halophyte Cakile maritima.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmtlGnsrg%3D&md5=4ecc4aedb6a27b19df89a549fda88189CAS |
Flowers TJ, Colmer TD (2008) Salinity tolerance in halophytes. New Phytologist 179, 945–963.
| Salinity tolerance in halophytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFWqur%2FE&md5=a36e6fda1d4e8df4e7a168c06e633bccCAS |
Flowers TJ, Yeo AR (1986) Ion relations of plants under drought and salinity. Functional Plant Biology 13, 75–91.
Flowers TJ, Troke PF, Yeo AR (1977) The mechanism of salt tolerance in halophytes. Annual Review of Plant Physiology 28, 89–121.
| The mechanism of salt tolerance in halophytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2sXksFSisb8%3D&md5=7709b2d492237493b7bb2d599b9d8622CAS |
Flowers TJ, Gaur PM, Gowda CL, Krishnamurthy L, Samineni S, Siddique KHM, Turner NC, Vadez V, Varshney RK, Colmer TD (2010) Salt sensitivity in chickpea. Plant, Cell & Environment 33, 490–509.
| Salt sensitivity in chickpea.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXltV2huro%3D&md5=2bb315bf360c2c99b54587500a20b6a5CAS |
Franke W (1982) Vitamin C in sea fennel (Crithmum maritimum), an edible wild plant. Economic Botany 36, 163–165.
| Vitamin C in sea fennel (Crithmum maritimum), an edible wild plant.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38Xkt1agtL4%3D&md5=65de5fe49535984ef5468f68e9a6e2b4CAS |
Ghanem ME, van Elteren J, Albacete A, Quinet M, Martínez-Andújar C, Kinet JM, Pérez-Alfocea F, Lutts S (2009) Impact of salinity on early reproductive physiology of tomato (Solanum lycopersicum) in relation to a heterogeneous distribution of toxic ions in flower organs. Functional Plant Biology 36, 125–136.
| Impact of salinity on early reproductive physiology of tomato (Solanum lycopersicum) in relation to a heterogeneous distribution of toxic ions in flower organs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsVaht7g%3D&md5=f557b0f8dbc65e48669401f006881173CAS |
Glenn EP, Brown JJ, Blumwald E (1999) Salt tolerance and crop potential of halophytes. Critical Reviews in Plant Sciences 18, 227–255.
| Salt tolerance and crop potential of halophytes.Crossref | GoogleScholarGoogle Scholar |
Grigore MN, Boscaiu M, Llinares J, Vicente O (2012) Mitigation of salt stress-induced inhibition of Plantago crassifolia reproductive development by supplemental calcium or magnesium. Notulae Botanicae Horti Agrobotanici Cluj-Napoca 40, 58–66.
Guo J, Suo S, 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=5348129b2f4cda45820e286450831259CAS |
Han N, Shao Q, Lu CM, Wang BS (2005) The leaf tonoplast V-H+-ATPase activity of a C3 halophyte Suaeda salsa is enhanced by salt stress in a Ca-dependent mode. Journal of Plant Physiology 162, 267–274.
| The leaf tonoplast V-H+-ATPase activity of a C3 halophyte Suaeda salsa is enhanced by salt stress in a Ca-dependent mode.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXktlantbY%3D&md5=6497a386ddfe43a0a9b2f97604921925CAS |
Khatun S, Flowers TJ (1995a) Effects of salinity on seed set in rice. Plant, Cell & Environment 18, 61–67.
| Effects of salinity on seed set in rice.Crossref | GoogleScholarGoogle Scholar |
Khatun S, Flowers TJ (1995b) The estimation of pollen viability in rice. Journal of Experimental Botany 46, 151–154.
| The estimation of pollen viability in rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXjslKhsrw%3D&md5=1fc5795f36b1cb29f4545c0a0ffc815eCAS |
Khatun S, Rizzo CA, Flowers TJ (1995) Genotypic variation in the effect of salinity on fertility in rice. Plant and Soil 173, 239–250.
| Genotypic variation in the effect of salinity on fertility in rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXnvVelu7s%3D&md5=3e16d0fad1fda808032c967e5f6df540CAS |
Kotula L, Khan HA, Quealy J, Turner NC, Vadez V, Siddique KHM, Clode P, Colmer TD (2015) Salt sensitivity in chickpea (Cicer arietinum L.): ions in reproductive tissues and yield components in contrasting genotypes. Plant, Cell & Environment 38, 1565–1577.
| Salt sensitivity in chickpea (Cicer arietinum L.): ions in reproductive tissues and yield components in contrasting genotypes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhtFGlsrnJ&md5=8be899418ee7583ab8339233bdc94e5fCAS |
Li PH, Wang ZL, Zhang H, Wang BS (2004) Cloning and expression analysis of the B subunit of V-H+-ATPase in the leaves of Suaeda salsa under NaCl stress. Acta Botanica Sinica 46, 93–99.
Li W, Liu X, Khan MA, Yamaguchi S (2005) The effect of plant growth regulators, nitric oxide, nitrate, 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, nitrate, 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=a7f8578d93c43c9d9b5d55fea1d261efCAS |
Li K, Wang Y, Han C, Zhang W, Jia H, Li X (2007) GA signaling and CO/FT regulatory module mediate salt-induced late flowering in Arabidopsis thaliana. Plant Growth Regulation 53, 195–206.
| GA signaling and CO/FT regulatory module mediate salt-induced late flowering in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXht1ahs7jJ&md5=7df5222ef4ef4b80c6cae337d98024e1CAS |
Lu C, Qiu N, Wang B, Zhang J (2003) Salinity treatment shows no effects on photosystem II photochemistry, but increases the resistance of photosystem II to heat stress in halophyte Suaeda salsa. Journal of Experimental Botany 54, 851–860.
| Salinity treatment shows no effects on photosystem II photochemistry, but increases the resistance of photosystem II to heat stress in halophyte Suaeda salsa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXit1aqsrw%3D&md5=184a498ff1d10f7f7727a4ea32b333a0CAS |
Mamo T, Richter C, Heiligtag B (1996) Salinity effects on the growth and ion concentrations of some chickpea (Cicer arietinum) and lentil (Lens culinaris medic) varieties. Journal Agronomy & Crop Science 176, 235–247.
| Salinity effects on the growth and ion concentrations of some chickpea (Cicer arietinum) and lentil (Lens culinaris medic) varieties.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XltlCgtL8%3D&md5=f6bbbd13afbba91c7eb4dd8f9c39fce8CAS |
Martin FW (1959) Staining and observing pollen tubes in the style by means of fluorescence. Biotechnic & Histochemistry 34, 125–128.
Mori S, Suzuki K, Oda R, Higuchi K, Maeda Y, Yoshiba M, Tadano T (2011) Characteristics of Na+ and K+ absorption in Suaeda salsa (L.) Pall. Soil Science and Plant Nutrition 57, 377–386.
| Characteristics of Na+ and K+ absorption in Suaeda salsa (L.) Pall.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtFCrurbJ&md5=3a7071614db5bac4f0ea5da8bba6a78eCAS |
Mullins PH, Marks TC (1987) Flowering phenology and seed production of Spartina anglica. Journal of Ecology 75, 1037–1048.
| Flowering phenology and seed production of Spartina anglica.Crossref | GoogleScholarGoogle Scholar |
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=b30f07d810b3303a6dcacfac2b459d6cCAS |
Onyemaobi I, Liu H, Siddique KHM, Yan G (2017) Both male and female malfunction contributes to yield reduction under water stress during meiosis in bread wheat. Frontiers in Plant Science 7, 1–11.
| Both male and female malfunction contributes to yield reduction under water stress during meiosis in bread wheat.Crossref | GoogleScholarGoogle Scholar |
Pang CH, Zhang SJ, Gong ZZ, Wang BS (2005) NaCl treatment markedly enhances H2O2-scavenging system in leaves of halophyte Suaeda salsa L. Physiologia Plantarum 124, 490–499.
Pang CH, Li K, Wang B (2011) Overexpression of SsCHLAPXs confers protection against oxidative stress induced by high light in transgenic Arabidopsis thaliana. Physiologia Plantarum 143, 355–366.
| Overexpression of SsCHLAPXs confers protection against oxidative stress induced by high light in transgenic Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsFehs7fO&md5=d3909c7175a9bc9e6024b47a9a049755CAS |
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=1f7aa66f09532f1534b2168575949745CAS |
Qiu N, Chen M, Guo J, Bao H, Ma X, Wang B (2007) Coordinate up-regulation of V-H+-ATPase and vacuolar Na+/H+ antiporter as a response to NaCl treatment in a C3 halophyte Suaeda salsa. Plant Science 172, 1218–1225.
| Coordinate up-regulation of V-H+-ATPase and vacuolar Na+/H+ antiporter as a response to NaCl treatment in a C3 halophyte Suaeda salsa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXkvFGitbo%3D&md5=4aafc44170ddec3f33d73171b904f0e3CAS |
Reddy PR, Goss JA (1971) Effect of salinity on pollen. I. Pollen viability as altered by increasing osmotic pressure with NaCl, MgCl2, and CaCl2. American Journal of Botany 58, 721–725.
| Effect of salinity on pollen. I. Pollen viability as altered by increasing osmotic pressure with NaCl, MgCl2, and CaCl2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE3MXltVKhsb0%3D&md5=5a640c0e013367260f00f9e0f1cd0fe7CAS |
Samineni S, Siddique KH, Gaur PM, Colmer TD (2011) Salt sensitivity of the vegetative and reproductive stages in chickpea (Cicer arietinum L.): podding is a particularly sensitive stage. Environmental and Experimental Botany 71, 260–268.
| Salt sensitivity of the vegetative and reproductive stages in chickpea (Cicer arietinum L.): podding is a particularly sensitive stage.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhvFWitL8%3D&md5=8514193d7c50cb92ca6389541bfc4a2aCAS |
Sedgley M (1977) Reduced pollen tube growth and the presence of callose in the pistil of the male floral stage of the avocado. Scientia Horticulturae 7, 27–36.
| Reduced pollen tube growth and the presence of callose in the pistil of the male floral stage of the avocado.Crossref | GoogleScholarGoogle Scholar |
Simopoulos AP (2004) Omega-3 fatty acids and antioxidants in edible wild plants. Biological Research 37, 263–277.
| Omega-3 fatty acids and antioxidants in edible wild plants.Crossref | GoogleScholarGoogle Scholar |
Sohrabi Y, Heidari G, Esmailpoor B (2008) Effect of salinity on growth and yield of desi and kabuli chickpea cultivars. Pakistan Journal of Biological Sciences 11, 664–667.
| Effect of salinity on growth and yield of desi and kabuli chickpea cultivars.Crossref | GoogleScholarGoogle Scholar |
Song J, Wang B (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 |
Song J, Fan H, Zhao Y, Jia Y, Du X, Wang B (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=0e1e3c257ca601623140453d3b80f597CAS |
Tardío J, Pardo-de-Santayana M, Morales R (2006) Ethnobotanical review of wild edible plants in Spain. Botanical Journal of the Linnean Society 152, 27–71.
| Ethnobotanical review of wild edible plants in Spain.Crossref | GoogleScholarGoogle Scholar |
Turner NC, Colmer TD, Quealy J, Pushpavalli R, Krishnamurthy L, Kaur J, Singh G, Siddique KHM, Vadez V (2013) Salinity tolerance and ion accumulation in chickpea (Cicer arietinum L.) subjected to salt stress. Plant and Soil 365, 347–361.
| Salinity tolerance and ion accumulation in chickpea (Cicer arietinum L.) subjected to salt stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXkslaktLw%3D&md5=832d17e60abe7cec5c74923172273341CAS |
Vadez V, Krishnamurthy L, Serraj R, Gaur PM, Upadhyaya HD, Hoisington DA, Varshney RK, Turner NC, Siddique KHM (2007) Large variation in salinity tolerance in chickpea is explained by differences in sensitivity at the reproductive stage. Field Crops Research 104, 123–129.
| Large variation in salinity tolerance in chickpea is explained by differences in sensitivity at the reproductive stage.Crossref | GoogleScholarGoogle Scholar |
Vadez V, Rashmi M, Sindhu K, Muralidharan M, Pushpavalli R, Turner NC, Krishnamurthy L, Gaur MP, Colmer TD (2012) Large number of flowers and tertiary branches, and higher reproductive success increase yields under salt stress in chickpea. European Journal of Agronomy 41, 42–51.
| Large number of flowers and tertiary branches, and higher reproductive success increase yields under salt stress in chickpea.Crossref | GoogleScholarGoogle Scholar |
Ventura Y, Sagi M (2013) Halophyte crop cultivation: the case for Salicornia and Sarcocornia. Environmental and Experimental Botany 92, 144–153.
| Halophyte crop cultivation: the case for Salicornia and Sarcocornia.Crossref | GoogleScholarGoogle Scholar |
Ventura Y, Myrzabayeva M, Alikulov Z, Omarov R, Khozin-Goldberg I, Sagi M (2014) Effects of salinity on flowering, morphology, biomass accumulation and leaf metabolites in an edible halophyte. AoB Plants 6, plu053
| Effects of salinity on flowering, morphology, biomass accumulation and leaf metabolites in an edible halophyte.Crossref | GoogleScholarGoogle Scholar |
Ventura Y, Eshel A, Pasternak D, Sagi M (2015) The development of halophyte-based agriculture: past and present. Annals of Botany 115, 529–540.
| The development of halophyte-based agriculture: past and present.Crossref | GoogleScholarGoogle Scholar |
Wagenvoort WA, van de Vooren JG, Brandenburg WA (1989) Plant domestication and the development of sea starwort (Aster tripolium L.) as a new vegetable crop. Acta Horticulturae 115–122.
| Plant domestication and the development of sea starwort (Aster tripolium L.) as a new vegetable crop.Crossref | GoogleScholarGoogle Scholar |
Wang BS, Lüttge U, Ratajczak R (2001) Effects of salt treatment and osmotic stress on V-ATPase and V-PPase in leaves of the halophyte Suaeda salsa. Journal of Experimental Botany 52, 2355–2365.
| Effects of salt treatment and osmotic stress on V-ATPase and V-PPase in leaves of the halophyte Suaeda salsa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXptVeisL0%3D&md5=ab2a637d7ccb22816ce1ac4d895f4bddCAS |
Yang MF, Song J, Wang BS (2010) Organ-specific responses of vacuolar H+-ATPase in the shoots and roots of C3 halophyte Suaeda salsa to NaCl. Journal of Integrative Plant Biology 52, 308–314.
| Organ-specific responses of vacuolar H+-ATPase in the shoots and roots of C3 halophyte Suaeda salsa to NaCl.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXksFCktL4%3D&md5=11b3d3772662569aaa0d1cca7a0a1831CAS |
Zhang QF, Li YY, Pang CH, Lu CM, Wang BS (2005) NaCl stress enhances thylakoid-bound SOD activity in the leaves of C3 halophyte Suaeda salsa L. Plant Science 168, 423–430.
| NaCl stress enhances thylakoid-bound SOD activity in the leaves of C3 halophyte Suaeda salsa L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVKksb3P&md5=329ebd74997367a1d11943e103cd8e3aCAS |
Zhao KF, Fan H, Ungar IA (2002) Survey of halophyte species in China. Plant Science 163, 491–498.
| Survey of halophyte species in China.Crossref | GoogleScholarGoogle Scholar |