The relationship between salt gland density and sodium accumulation/secretion in a wide selection from three Zoysia species
Akihiro Yamamoto A B , Masatsugu Hashiguchi A B , Ryo Akune A , Takahito Masumoto A , Melody Muguerza A , Yuichi Saeki A and Ryo Akashi A C
+ Author Affiliations
- Author Affiliations
A Faculty of Agriculture, University of Miyazaki, 1-1 Gakuen Kibanadai-nishi, Miyazaki, Miyazaki 889-2192, Japan.
B These authors contributed equally to this work.
C Corresponding author. Email: rakashi@cc.miyazaki-u.ac.jp
Australian Journal of Botany 64(4) 277-284 https://doi.org/10.1071/BT15261
Submitted: 19 November 2015 Accepted: 20 April 2016 Published: 17 June 2016
Abstract
Several zoysiagrasses (Zoysia spp.) have been reported to have leaf-epidermal salt glands, and it has been suggested that salt gland density, salt secretion and salt tolerance are positively correlated. The economically most important Zoysia species are Zoysia japonica Steud., Zoysia matrella Merr., and Zoysia pacifica (Goudswaard) M. Hotta & Kuroki, and among these, Z. matrella is considered to be the most salt-tolerant. In this study, we investigated the salt gland density, and characterised the secretion and accumulation of Na+ of 48 accessions of the three Zoysia species. We did not find any morphological differences in salt glands of Z. japonica and Z. pacifica, but large bicellular salt glands were found only on the adaxial side of Z. matrella. In addition, salt gland density differed significantly within and between the species. Under salt stress, all accessions accumulated and secreted Na+ at different rates. Z. japonica was a salt-accumulating type, whereas Z. matrella and Z. pacifica secreted most of the absorbed salt. However, the correlation between salt gland density and salt accumulation/secretion were not observed. Furthermore, Z. pacifica had the lowest gland density but showed the highest Na+ uptake and a secretion rate similar to most salt-tolerant Z. matrella. These results suggest that response to salt stress, namely, salt accumulation/secretion, is different between species, and that salt gland density and salt secretion are not always positively correlated.
Additional keywords: leaf blade, Na+ accumulation, Na+ secretion, salinity, salt glands, Zoysia spp.
References
Ahn JH, Kim JS, Kim S, Soh HY, Shin H, Jang H, Ryu JH, Kim A, Yun K-L, Kim S, Kim KS, Choi D, Huh JH (2015) De novo transcriptome analysis to identify anthocyanin biosynthesis genes responsible for tissue-specific pigmentation in zoysiagrass (Zoysia japonica Steud.) PLoS One 10, e0124497| De novo transcriptome analysis to identify anthocyanin biosynthesis genes responsible for tissue-specific pigmentation in zoysiagrass (Zoysia japonica Steud.)Crossref | GoogleScholarGoogle Scholar | 25905914PubMed |
Akamine H, Ishimine Y, Kurihara N, Omokawa H, Ichizen N, Kuramochi H (2002) Influence of salinity on the growth, and Na, K and amino acid contents in Mascarenegrass (Zoysia tenuifolia Willd.). Journal of Japanese Society of Turfgrass Science 31, 2–6. [in Japanese with English abstract]
Akiyoshi M, Yaneshita M, Nagasawa R, Endo N (1998) Seawater tolerance of zoysigrasses in relation to morphological and genetic classification. Journal of Japanese Society of Grassland Science 44, 7–13.
Alshammary SF (2013) Effect of salinity on ion relations of four turfgrasses. Journal of Food Agriculture and Environment 11, 1321–1326.
Apse MP, Blumwald E (2007) Na+ transport in plants. FEBS Letters 581, 2247–2254.
| Na+ transport in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXls1aiurY%3D&md5=80f679405db97caaccf63f74a1a06405CAS | 17459382PubMed |
Bassil E, Blumwald E (2014) The ins and outs of intracellular ion homeostasis: NHX-type cation/H+ transporters. Current Opinion in Plant Biology 22, 1–6.
| The ins and outs of intracellular ion homeostasis: NHX-type cation/H+ transporters.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhsVyhsLjP&md5=08fa83503c775900e91a1b8adedda64dCAS | 25173972PubMed |
Blumwald E, Aharon GS, Apse MP (2000) Sodium transport in plant cells. Biochimica et Biophysica Acta 1465, 140–151.
| Sodium transport in plant cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXit1Wgtrs%3D&md5=b9c544a64cc4aa2d99c4028bee4c5a18CAS | 10748251PubMed |
Bohnert HJ, Nelson DE, Jensen RG (1995) Adaptations to environmental stresses. The Plant Cell 7, 1099–1111.
| Adaptations to environmental stresses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXnt1Sgt7Y%3D&md5=364ff523575d416e55b34f203842bc9dCAS | 12242400PubMed |
Boyer JS (1982) Plant productivity and environment. Science 218, 443–448.
| Plant productivity and environment.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cvjvVahuw%3D%3D&md5=c831b70709d52511ea07ada5f2e37863CAS | 17808529PubMed |
Brede D (2000) ‘Turfgrass maintenance reduction handbook: sports, lawns, and golf.’ (Sleeping Bear Press: Chelsea, MI, USA)
Céccoli C, Ramos J, Pilatti V, Dellaferrera I, Tivano JC, Taleisnik E, Vegetti AC (2015) Salt glands in the Poaceae family and their relationship to salinity tolerance. Botanical Review 81, 162–178.
| Salt glands in the Poaceae family and their relationship to salinity tolerance.Crossref | GoogleScholarGoogle Scholar |
Emmons R (1995) ‘Turf grass science and management.’ (2nd edn) (Delmar Publishers: New York)
Engelke MC, Anderson S (2003) Zoysiagrass (Zoysia spp.). In ‘Turfgrass biology, genetics, and breeding’. (Eds MD Casler, RR Duncan) pp. 271–285. (Wiley: Hoboken, NJ, USA)
Engelke MC, Colbaugh PF, Reinert JA, Marcum KB, White RH, Ruemmele B, Anderson SJ (2002a) Registration of ‘Diamond’ zoysiagrass. Crop Science 42, 304–305.
| Registration of ‘Diamond’ zoysiagrass.Crossref | GoogleScholarGoogle Scholar | 11756296PubMed |
Engelke MC, Reinert JA, Colbaugh PF, White RH, Ruemmele B, Marcum KB, Anderson SJ (2002b) Registration of ‘Cavalier’ zoysiagrass. Crop Science 42, 302–303.
| Registration of ‘Cavalier’ zoysiagrass.Crossref | GoogleScholarGoogle Scholar | 11756294PubMed |
Faraday CD, Thomson WW (1986) Functional aspects of the salt glands of the Plumbaginaceae. Journal of Experimental Botany 37, 1129–1135.
| Functional aspects of the salt glands of the Plumbaginaceae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28Xls12itbk%3D&md5=f3eee66321184447062fee6e034e443eCAS |
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=d9f2209b6b23155fd1513599e6623e58CAS | 18565144PubMed |
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=4f872964f0475cac7cde42ba81987b11CAS |
Flowers TJ, Galal HK, Bromham L (2010) Evolution of halophytes: multiple origins of salt tolerance in land plants. Functional Plant Biology 37, 604–612.
| Evolution of halophytes: multiple origins of salt tolerance in land plants.Crossref | GoogleScholarGoogle Scholar |
Gao Z, He X, Zhao B, Zhou C, Liang Y, Ge R, Shen Y, Huang Z (2010) Overexpressing a putative aquaporin gene from wheat, TaNIP, enhances salt tolerance in transgenic Arabidopsis. Plant & Cell Physiology 51, 767–775.
| Overexpressing a putative aquaporin gene from wheat, TaNIP, enhances salt tolerance in transgenic Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXmtFOgsLo%3D&md5=f4157eb34e6c180306a6c654656a8de6CAS |
Greenway H, Munns RA (1980) Mechanisms of salt tolerance in nonhalophytes. Annual Review of Plant Physiology 31, 149–190.
| Mechanisms of salt tolerance in nonhalophytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3cXksVWntb4%3D&md5=ed0b5f6fd679cb50a88f296bc53e78abCAS |
Guo H, Ding W, Chen J, Chen X, Zheng Y, Wang Z, Liu J (2014) Genetic linkage map construction and QTL mapping of salt tolerance traits in zoysiagrass (Zoysia japonica). PLoS One 9, e107249
| Genetic linkage map construction and QTL mapping of salt tolerance traits in zoysiagrass (Zoysia japonica).Crossref | GoogleScholarGoogle Scholar | 25203715PubMed |
Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annual Review of Plant Physiology and Plant Molecular Biology 51, 463–499.
| Plant cellular and molecular responses to high salinity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXlsVymt7s%3D&md5=fad38c5c1f8e08ad724bd48827f6943fCAS | 15012199PubMed |
Hashiguchi M, Tsuruta S, Matsuo T, Akamine H, Akashi R (2006) Analysis of genetic resource in Zoysia spp. 1. Morphological characteristics and covering gain in zoysiagrass indigenous to Southwest Islands of Japan. Japanese Journal of Grassland Science 52, 183–189. [in Japanese with English abstract]
Hashiguchi M, Tsuruta S, Matsuo T, Ebina M, Kobayashi M, Akamine H, Akashi R (2007) Analysis of genetic resource in Zoysia spp. 2. Evaluation of genetic diversity in zoysiagrass indigenous to Southwest Islands of Japan based on simple sequence repeat makers. Japanese Journal of Grassland Science 53, 133–137. [in Japanese with English abstract]
Kasuga M, Liu Q, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1999) Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor. Nature Biotechnology 17, 287–291.
| Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXhs1Chu78%3D&md5=d608788916b43f6f610555efae967944CAS | 10096298PubMed |
Kim YH, Shim IS, Kobayashi K, Usui K (1999) Relationship between Na content or K/Na ratio in shoots and salt tolerance in several gramineous plants. Journal of Weed Science and Technology 44, 293–299.
| Relationship between Na content or K/Na ratio in shoots and salt tolerance in several gramineous plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXmsFKhsA%3D%3D&md5=040c03b097156a422961204d8b1cdfddCAS |
Kimball JA, Zuleta CM, Kenworthy KE, Lehman VG, Harris-Shultz KR, Milla-Lewis SR (2013) Genetic relationships in Zoysia species and the identification of putative interspecific hybrids using simple sequence repeat markers and inflorescence traits. Crop Science 53, 285–295.
| Genetic relationships in Zoysia species and the identification of putative interspecific hybrids using simple sequence repeat markers and inflorescence traits.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXnsVOltbc%3D&md5=cf0678daa3ebfe021e8a78771a61589dCAS |
Kobayashi H (2008) Ion secretion via salt glands in Poaceae. Japanese Journal of Plant Science 2, 1–8.
Kramer D (1983) The possible role of transfer cells in the adaptation of plants to salinity. Physiologia Plantarum 58, 549–555.
| The possible role of transfer cells in the adaptation of plants to salinity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXltVahsLc%3D&md5=0c74d29c73a10accd0695f9685967bc2CAS |
Kronzucker H, Britto D (2011) Sodium transport in plants: a critical review. New Phytologist 189, 54–81.
| Sodium transport in plants: a critical review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXltlGhug%3D%3D&md5=3a4143ba193d4de840fbc6ea4d17f390CAS | 21118256PubMed |
Liphschitz N, Waisel Y (1974) Existence of salt glands in various genera of the Gramineae. New Phytologist 73, 507–513.
| Existence of salt glands in various genera of the Gramineae.Crossref | GoogleScholarGoogle Scholar |
Marcum KB (1999) Salinity tolerance mechanisms of grasses in the subfamily Chloridoideae. Crop Science 39, 1153–1160.
| Salinity tolerance mechanisms of grasses in the subfamily Chloridoideae.Crossref | GoogleScholarGoogle Scholar |
Marcum KB, Murdoch CL (1990) Salt glands in the Zoysieae. Annals of Botany 66, 1–7.
Marcum KB, Murdoch CL (1994) Salinity tolerance mechanisms of six C4 turfgrasses. Journal of the American Society for Horticultural Science 119, 779–784.
Marcum KB, Anderson SJ, Engelke MC (1998) Salt gland ion secretion: a salinity tolerance mechanism among five zoysiagrass species. Crop Science 38, 806–810.
| Salt gland ion secretion: a salinity tolerance mechanism among five zoysiagrass species.Crossref | GoogleScholarGoogle Scholar |
Marcum KB, Wess G, Ray DT, Engelke MC (2003) Zoysiagrasses, salt glands, and salt tolerance. USGA Turfgrass and Environmental Research Online 2, 1–6.
Moinuddin M, Gulzar S, Ahmed MZ, Gul B, Koyro H-W, Khan MA (2014) Excreting and non-excreting grasses exhibit different salt resistance strategies. AoB Plants 6, plu038
| Excreting and non-excreting grasses exhibit different salt resistance strategies.Crossref | GoogleScholarGoogle Scholar | 24996428PubMed |
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=b74112ae115ff11efb10a374e7a22a5aCAS | 18444910PubMed |
Nakahara Y, Sawabe S, Kainuma K, Katsuhara M, Shibasaka M, Yamamoto K, Oguri S, Sakamoto H (2015) Yeast functional screen to identify genes conferring salt stress tolerance in Salicornia europaea. Frontiers in Plant Science 6, 920
| Yeast functional screen to identify genes conferring salt stress tolerance in Salicornia europaea.Crossref | GoogleScholarGoogle Scholar | 26579166PubMed |
Oi T, Hirunagi K, Taniguchi M, Miyake H (2013) Salt excretion from the salt glands in Rhodes grass (Chloris gayana Kunth) as evidenced by low-vacuum scanning electron microscopy. Flora 208, 52–57.
| Salt excretion from the salt glands in Rhodes grass (Chloris gayana Kunth) as evidenced by low-vacuum scanning electron microscopy.Crossref | GoogleScholarGoogle Scholar |
Pollak G, Waisel Y (1970) Salt secretion in Aeluropus litoralis (Willd.) Parl. Annals of Botany 34, 879–888.
Qian YL, Engelke MC, Foster MJ (2000) Salinity effects on zoysiagrass cultivars and experimental lines. Crop Science 40, 488–492.
| Salinity effects on zoysiagrass cultivars and experimental lines.Crossref | GoogleScholarGoogle Scholar |
Rao S (2011) Elucidation of mechanisms of salinity tolerance in Zoysia matrella cultivars – a study of structure and function of salt glands. PhD thesis. Texas A&M University
Salama FM, El-Naggar SM, Ramadan T (1999) Salt glands of some halophytes in Egypt. Phyton 39, 91–105.
Sanadhya P, Agarwal P, Agarwal PK (2015) Ion homeostasis in a salt-secreting halophytic grass. AoB Plants 7, plv055
| Ion homeostasis in a salt-secreting halophytic grass.Crossref | GoogleScholarGoogle Scholar | 25990364PubMed |
Smirnoff N (1998) Plant resistance to environmental stress. Current Opinion in Biotechnology 9, 214–219.
| Plant resistance to environmental stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXjtFeht7s%3D&md5=78a2b8b6b72a3fa179b4e7e5c9c7e26bCAS | 9664051PubMed |
Tan WK, Lim TK, Loh CS, Kumar P, Lin Q (2015) Proteomic characterization of the salt gland-enriched tissues of the mangrove tree species Avicennia officinalis. PLoS One 10, e0133386
| Proteomic characterization of the salt gland-enriched tissues of the mangrove tree species Avicennia officinalis.Crossref | GoogleScholarGoogle Scholar | 26193361PubMed |
Tanaka H, Tokunaga R, Muguerza M, Kitazaki Y, Hashiguchi M, Sato S, Tabata S, Akashi R (2016a) Genetic structure and speciation of zoysiagrass ecotypes collected in Japan. Crop Science 56, 818–826.
| Genetic structure and speciation of zoysiagrass ecotypes collected in Japan.Crossref | GoogleScholarGoogle Scholar |
Tanaka H, Hirakawa H, Muguerza M, Tabata S, Akashi R, Sato S (2016b) The complete chloroplast genome sequence of Zoysia matrella. Crop Science 56, 1206–1212.
| The complete chloroplast genome sequence of Zoysia matrella.Crossref | GoogleScholarGoogle Scholar |
Tanaka H, Hirakawa H, Kosugi S, Nakayama S, Ono A, Watanabe A, Hashiguchi M, Gondo T, Ishigaki G, Muguerza M, Shimizu K, Sawamura N, Inoue T, Shigeki Y, Ohno N, Tabata S, Akashi R, Sato S (2016c) Sequencing and comparative analyses of the genomes of zoysiagrasses. DNA Research 23, 171–180.
| Sequencing and comparative analyses of the genomes of zoysiagrasses.Crossref | GoogleScholarGoogle Scholar | 26975196PubMed |
Uddin MK, Juraimi AJ (2013) Salinity tolerance turfgrass: history and prospects. Scientific World Journal 2013, 409413
| Salinity tolerance turfgrass: history and prospects.Crossref | GoogleScholarGoogle Scholar | 24222734PubMed |
Wang F, Singh R, Genovesi AD, Wai CM, Huang X, Chandra A, Yu Q (2015) Sequence-tagged high-density genetic maps of Zoysia japonica provide insights into genome evolution in Chloridoideae. The Plant Journal 82, 744–757.
| Sequence-tagged high-density genetic maps of Zoysia japonica provide insights into genome evolution in Chloridoideae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXovV2qu7o%3D&md5=43cca012484bb32c5102099ed0e23b31CAS | 25846381PubMed |
Wei S, Du Z, Gao F, Ke X, Li J, Liu J, Zhou Y (2015) Global transcriptome profiles of ‘Meyer’ zoysiagrass in response to cold stress. PLoS One 10, e0131153
| Global transcriptome profiles of ‘Meyer’ zoysiagrass in response to cold stress.Crossref | GoogleScholarGoogle Scholar | 26115186PubMed |
Xiao B, Huang Y, Tang N, Xiong L (2007) Over-expression of a LEA gene in rice improves drought resistance under the field conditions. Theoretical and Applied Genetics 115, 35–46.
| Over-expression of a LEA gene in rice improves drought resistance under the field conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXls1Sgsrk%3D&md5=f1a463ddc843b6919f550768a17c7bd4CAS | 17426956PubMed |
Xie Q, Niu J, Xu X, Xu L, Zhang Y, Fan B, Liang X, Zhang L, Yin S, Han L (2015) De novo assembly of the Japanese lawngrass (Zoysia japonica Steud.) root transcriptome and identification of candidate unigenes related to early responses under salt stress. Frontiers in Plant Science 6, 610
| De novo assembly of the Japanese lawngrass (Zoysia japonica Steud.) root transcriptome and identification of candidate unigenes related to early responses under salt stress.Crossref | GoogleScholarGoogle Scholar | 26347751PubMed |
Yamamoto A, Shim IS, Fujihara S, Yoneyama T, Usui K (2003) Physiochemical factors affecting the salt tolerance of Echinochloa crus-galli Beauv. var. formosensis Ohwi. Weed Biology and Management 3, 98–104.
| Physiochemical factors affecting the salt tolerance of Echinochloa crus-galli Beauv. var. formosensis Ohwi.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXmtVOjtr0%3D&md5=6a531d740c4683b999bb38cacfcf0473CAS |
Yancey PH, Clark ME, Hand SC, Bowlus PD, Somero GN (1982) Living with water stress: evolution of osmolyte systems. Science 217, 1214–1222.
| Living with water stress: evolution of osmolyte systems.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38XlsFyisbw%3D&md5=9ede73411b2464d3f1f5a6eaf590ba39CAS | 7112124PubMed |
Zouhaier B, Abdallah A, Najla T, Wahbi D, Wided C, Aouatef BA, Chedly A, Abderazzak S (2015) Scanning and transmission electron microscopy and X-ray analysis of leaf salt glands of Limoniastrum guyonianum Boiss. under NaCl salinity. Micron 78, 1–9.
| Scanning and transmission electron microscopy and X-ray analysis of leaf salt glands of Limoniastrum guyonianum Boiss. under NaCl salinity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhtVyhs77K&md5=58ba9d7dde473b726256f6438c31e6faCAS | 26102605PubMed |
