Proto Kranz-like leaf traits and cellular ionic regulation are associated with salinity tolerance in a halophytic wild rice

Springer Science and Business Media LLC - Tập 2 - Trang 1-19 - 2022
Miing-Tiem Yong1, Celymar Angela Solis1,2, Samuel Amatoury1, Gothandapani Sellamuthu3, Raja Rajakani3, Michelle Mak1, Gayatri Venkataraman3, Lana Shabala2, Meixue Zhou2, Oula Ghannoum4, Paul Holford1, Samsul Huda1, Sergey Shabala5,2, Zhong-Hua Chen1,4
1School of Science, Western Sydney University, Penrith, Australia
2Tasmanian Institute of Agriculture, College of Science and Engineering, University of Tasmania, Hobart, Australia
3Plant Molecular Biology Laboratory, M. S. Swaminathan Research Foundation, III Cross Street, Taramani Institutional Area, Chennai, India
4Hawkesbury Institute for the Environment, Western Sydney University, Penrith, Australia
5International Research Centre for Environmental Membrane Biology, Foshan University, Foshan, China

Tóm tắt

Species of wild rice (Oryza spp.) possess a wide range of stress tolerance traits that can be potentially utilized in breeding climate-resilient cultivated rice cultivars (Oryza sativa) thereby aiding global food security. In this study, we conducted a greenhouse trial to evaluate the salinity tolerance of six wild rice species, one cultivated rice cultivar (IR64) and one landrace (Pokkali) using a range of electrophysiological, imaging, and whole-plant physiological techniques. Three wild species (O. latifolia, O. officinalis and O. coarctata) were found to possess superior salinity stress tolerance. The underlying mechanisms, however, were strikingly different. Na+ accumulation in leaves of O. latifolia, O. officinalis and O. coarctata were significantly higher than the tolerant landrace, Pokkali. Na+ accumulation in mesophyll cells was only observed in O. coarctata, suggesting that O. officinalis and O. latifolia avoid Na+ accumulation in mesophyll by allocating Na+ to other parts of the leaf. The finding also suggests that O. coarctata might be able to employ Na+ as osmolyte without affecting its growth. Further study of Na+ allocation in leaves will be helpful to understand the mechanisms of Na+ accumulation in these species. In addition, O. coarctata showed Proto Kranz-like leaf anatomy (enlarged bundle sheath cells and lower numbers of mesophyll cells), and higher expression of C4-related genes (e.g., NADPME, PPDK) and was a clear outlier with respect to salinity tolerance among the studied wild and cultivated Oryza species. The unique phylogenetic relationship of O. coarctata with C4 grasses suggests the potential of this species for breeding rice with high photosynthetic rate under salinity stress in the future.

Tài liệu tham khảo

Adem GD, Chen G, Shabala L, Chen Z-H, Shabala S (2020) GORK channel: a master switch of plant metabolism? Trends Plant Sci 25(5):434–445. https://doi.org/10.1016/j.tplants.2019.12.012 Babla MH, Tissue DT, Cazzonelli CI, Chen Z-H (2020) Effect of high light on canopy-level photosynthesis and leaf mesophyll ion flux in tomato. Planta 252(5):80. https://doi.org/10.1007/s00425-020-03493-0 Bassil E, Tajima H, Liang Y-C, M-a O, Ushijima K, Nakano R, Esumi T, Coku A, Belmonte M, Blumwald E (2011) The Arabidopsis Na+/H+ antiporters NHX1 and NHX2 control vacuolar pH and K+ homeostasis to regulate growth, flower development, and reproduction. Plant Cell 23(9):3482–3497. https://doi.org/10.1105/tpc.111.089581 Berry JO, Mure CM, Yerramsetty P (2016) Regulation of rubisco gene expression in C4 plants. Curr Opin Plant Biol 31:23–28. https://doi.org/10.1016/j.pbi.2016.03.004 Bromham L, Bennett TH (2014) Salt tolerance evolves more frequently in C4 grass lineages. J Evol Biol 27(3):653–659. https://doi.org/10.1111/jeb.12320 Bromham L, Hua X, Cardillo M (2020) Macroevolutionary and macroecological approaches to understanding the evolution of stress tolerance in plants. Plant Cell Environ 43(12):2832–2846. https://doi.org/10.1111/pce.13857 Caperta AD, Róis AS, Teixeira G, Garcia-Caparros P, Flowers TJ (2020) Secretory structures in plants: lessons from the Plumbaginaceae on their origin, evolution and roles in stress tolerance. Plant Cell Environ 43(12):2912–2931. https://doi.org/10.1111/pce.13825 Chatterjee J, Dionora J, Elmido-Mabilangan A, Wanchana S, Thakur V, Bandyopadhyay A, Brar DS, Quick WP (2016) The evolutionary basis of naturally diverse rice leaves anatomy. PLoS ONE 11(10):e0164532. https://doi.org/10.1371/journal.pone.0164532 Chen G, Hu Q, Luo L, Yang T, Zhang S, Hu Y, Yu L, Xu G (2015) Rice potassium transporter OsHAK1 is essential for maintaining potassium-mediated growth and functions in salt tolerance over low and high potassium concentration ranges. Plant Cell Environ 38(12):2747–2765. https://doi.org/10.1111/pce.12585 Chen T, Zhu Y, Chen K, Shen C, Zhao X, Shabala S, Shabala L, Meinke H, Venkataraman G, Chen ZH (2020) Identification of new QTL for salt tolerance from rice variety Pokkali. J Agron Crop Sci 206(2):202–213. https://doi.org/10.1111/jac.12387 Chen Z, Cuin TA, Zhou M, Twomey A, Naidu BP, Shabala S (2007) Compatible solute accumulation and stress-mitigating effects in barley genotypes contrasting in their salt tolerance. J Exp Bot 58(15–16):4245–4255. https://doi.org/10.1093/jxb/erm284 Chen Z, Soltis DE (2020) Evolution of environmental stress responses in plants. Plant, Cell and Environment, pp 2827–2831. https://doi.org/10.1111/pce.13922 Che-Othman MH, Millar AH, Taylor NL (2017) Connecting salt stress signalling pathways with salinity-induced changes in mitochondrial metabolic processes in C3 plants. Plant Cell Environ 40(12):2875–2905. https://doi.org/10.1111/pce.13034 Christin P-A, Osborne CP, Chatelet DS, Columbus JT, Besnard G, Hodkinson TR, Garrison LM, Vorontsova MS, Edwards EJ (2013) Anatomical enablers and the evolution of C4 photosynthesis in grasses. Proc Natl Acad Sci 110(4):1381–1386. https://doi.org/10.1073/pnas.1216777110 Edwards EJ, Osborne CP, Stromberg CA, Smith SA, Consortium CG (2010) The origins of C4 grasslands: integrating evolutionary and ecosystem science. Science 328:587–591 Ermakova M, Danila FR, Furbank RT, von Caemmerer S (2020) On the road to C4 rice: advances and perspectives. Plant J 101(4):940–950. https://doi.org/10.1111/tpj.14562 Feng X, Liu W, Qiu CW, Zeng F, Wang Y, Zhang G, Chen ZH, Wu F (2020) HvAKT2 and HvHAK1 confer drought tolerance in barley through enhanced leaf mesophyll H+ homoeostasis. Plant Biotechnol J 18(8):1683–1696. https://doi.org/10.1111/pbi.13332 Flowers TJ, Galal HK, Bromham L (2010) Evolution of halophytes: multiple origins of salt tolerance in land plants. Funct Plant Biol 37(7):604–612. https://doi.org/10.1071/FP09269 Ganeshan P, Jain A, Parmar B, Rao A, Sreenu K, Mishra P, Mesapogu S, Subrahmanyam D, Ram T, Sarla N (2016) Identification of salt-tolerant rice lines among interspecific BILs developed by crossing Oryza sativa x O. rufipogon and O. sativa x O. nivara. Aust J Crop Sci 10(2):220 Ge S, Sang T, Lu B-R, Hong D-Y (2001) Phylogeny of the genus Oryza as revealed by molecular approaches. Rice Genetics IV. World Scientific, pp 89–105 https://doi.org/10.1142/9789812814296_0006 Gerona MEB, Deocampo MP, Egdane JA, Ismail AM, Dionisio-Sese ML (2019) Physiological responses of contrasting rice genotypes to salt stress at reproductive stage. Rice Sci 26(4):207–219. https://doi.org/10.1016/j.rsci.2019.05.001 Ghannoum O, Evans JR, Chow WS, Andrews TJ, Conroy JP, von Caemmerer S (2005) Faster rubisco is the key to superior nitrogen-use efficiency in NADP-malic enzyme relative to NAD-malic enzyme C4 grasses. Plant Physiol 137(2):638–650. https://doi.org/10.1104/pp.104.054759 Grieve BD, Duckett T, Collison M, Boyd L, West J, Yin H, Arvin F, Pearson S (2019) The challenges posed by global broadacre crops in delivering smart Agri-robotic solutions: a fundamental rethink is required. Glob Food Secur 23:116–124. https://doi.org/10.1016/j.gfs.2019.04.011 Hamamoto S, Horie T, Hauser F, Deinlein U, Schroeder JI, Uozumi N (2015) HKT transporters mediate salt stress resistance in plants: from structure and function to the field. Curr Opin Biotechnol 32:113–120. https://doi.org/10.1016/j.copbio.2014.11.025 Hanin M, Ebel C, Ngom M, Laplaze L, Masmoudi K (2016) New insights on plant salt tolerance mechanisms and their potential use for breeding. Front Plant Sci 7:1787. https://doi.org/10.3389/fpls.2016.01787 Hatch MD (1987) C4 photosynthesis: a unique elend of modified biochemistry, anatomy and ultrastructure. Biochimica et Biophysica Acta (BBA) - Rev Bioenerg 895(2):81–106. https://doi.org/10.1016/S0304-4173(87)80009-5 Hibberd JM, Covshoff S (2010) The regulation of gene expression required for C4 photosynthesis. Annu Rev Plant Biol 61(1):181–207. https://doi.org/10.1146/annurev-arplant-042809-112238 Huertas R, Olias R, Eljakaoui Z, Gálvez FJ, Li J, De Morales PA, Belver A, Rodríguez-Rosales MP (2012) Overexpression of SlSOS2 (SlCIPK24) confers salt tolerance to transgenic tomato. Plant Cell Environ 35(8):1467–1482. https://doi.org/10.1111/j.1365-3040.2012.02504.x Ji H, Pardo JM, Batelli G, Van Oosten MJ, Bressan RA, Li X (2013) The salt overly sensitive (SOS) pathway: established and emerging roles. Mol Plant 6(2):275–286. https://doi.org/10.1093/mp/sst017 Kavitha P, Miller A, Mathew M, Maathuis FJ (2012) Rice cultivars with differing salt tolerance contain similar cation channels in their root cells. J Exp Bot 63(8):3289–3296. https://doi.org/10.1093/jxb/ers052 Khatun S, Flowers T (1995) Effects of salinity on seed set in rice. Plant Cell Environ 18(1):61–67. https://doi.org/10.1111/j.1365-3040.1995.tb00544.x Kobayashi NI, Yamaji N, Yamamoto H, Okubo K, Ueno H, Costa A, Tanoi K, Matsumura H, Fujii-Kashino M, Horiuchi T (2017) OsHKT1;5 mediates Na+ exclusion in the vasculature to protect leaf blades and reproductive tissues from salt toxicity in rice. Plant J 91(4):657–670. https://doi.org/10.1111/tpj.13595 Kotula L, Clode PL, Jimenez JDLC, Colmer TD (2019) Salinity tolerance in chickpea is associated with the ability to ‘exclude’ Na from leaf mesophyll cells. J Exp Bot 70(18):4991–5002. https://doi.org/10.1093/jxb/erz241 Kotula L, Garcia Caparros P, Zörb C, Colmer TD, Flowers TJ (2020) Improving crop salt tolerance using transgenic approaches: an update and physiological analysis. Plant Cell Environ 43(12):2932–2956. https://doi.org/10.1111/pce.13865 Kovach MJ, Sweeney MT, McCouch SR (2007) New insights into the history of rice domestication. Trends Genet 23(11):578–587. https://doi.org/10.1016/j.tig.2007.08.012 Kronzucker HJ, Britto DT (2011) Sodium transport in plants: a critical review. New Phytol 189(1):54–81. https://doi.org/10.1111/j.1469-8137.2010.03540.x Ku MS, Monson RK, Littlejohn RO, Nakamoto H, Fisher DB, Edwards GE (1983) Photosynthetic characteristics of C3-C4 intermediate Flaveria species: I. leaf anatomy, photosynthetic responses to O2 and CO2, and activities of key enzymes in the C3 and C4 pathways. Plant Physiol 71(4):944–948. https://doi.org/10.1104/pp.71.4.944 Kumar V, Khare T (2015) Individual and additive effects of Na+ and cl− ions on rice under salinity stress. Arch Agron Soil Sci 61(3):381–395. https://doi.org/10.1080/03650340.2014.936400 Laisk AK (1977) Kinetics of photosynthesis and photorespiration of C3 in plants. FAO Lakra N, Kaur C, Anwar K, Singla-Pareek SL, Pareek A (2018) Proteomics of contrasting rice genotypes: identification of potential targets for raising crops for saline environment. Plant Cell Environ 41(5):947–969. https://doi.org/10.1111/pce.12946 Lichtenthaler HK, Buschmann C (2001) Chlorophylls and carotenoids: measurement and characterization by UV-VIS spectroscopy. Curr Protoc Food Anal Chem 1(1):F4.3.1–F4.3.8. https://doi.org/10.1002/0471142913.faf0403s01 Liu J, Shabala S, Shabala L, Zhou M, Meinke H, Venkataraman G, Chen Z, Zeng F, Zhao Q (2019) Tissue-specific regulation of Na+ and K+ transporters explains genotypic differences in salinity stress tolerance in rice. Front Plant Sci 10:1361. https://doi.org/10.3389/fpls.2019.01361 Liu X, Cai S, Wang G, Wang F, Dong F, Mak M, Holford P, Ji J, Salih A, Zhou M (2017a) Halophytic NHXs confer salt tolerance by altering cytosolic and vacuolar K+ and Na+ in Arabidopsis root cell. Plant Growth Regul 82(2):333–351. https://doi.org/10.1007/s10725-017-0262-7 Liu X, Fan Y, Mak M, Babla M, Holford P, Wang F, Chen G, Scott G, Wang G, Shabala S, Zhou M, Chen Z-H (2017b) QTLs for stomatal and photosynthetic traits related to salinity tolerance in barley. BMC Genomics 18(1):9. https://doi.org/10.1186/s12864-016-3380-0 Liu X, Mak M, Babla M, Wang F, Chen G, Veljanoski F, Wang G, Shabala S, Zhou M, Chen Z-H (2014) Linking stomatal traits and expression of slow anion channel genes HvSLAH1 and HvSLAC1 with grain yield for increasing salinity tolerance in barley. Front Plant Sci 5:634. https://doi.org/10.3389/fpls.2014.00634 Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408 Lutts S, Kinet JM, Bouharmont J (1996) NaCl-induced senescence in leaves of Rice ( Oryza sativa L.) cultivars differing in salinity resistance. Ann Bot 78(3):389–398. https://doi.org/10.1006/anbo.1996.0134 Mak M, Babla M, Xu S-C, O’Carrigan A, Liu X-H, Gong Y-M, Holford P, Chen Z-H (2014) Leaf mesophyll K+, H+ and Ca2+ fluxes are involved in drought-induced decrease in photosynthesis and stomatal closure in soybean. Environ Exp Bot 98:1–12. https://doi.org/10.1016/j.envexpbot.2013.10.003 Malagoli P, Britto DT, Schulze LM, Kronzucker HJ (2008) Futile Na+ cycling at the root plasma membrane in rice (Oryza sativa L.): kinetics, energetics, and relationship to salinity tolerance. J Exp Bot 59(15):4109–4117. https://doi.org/10.1093/jxb/ern249 Mangano S, Silberstein S, Santa-María GE (2008) Point mutations in the barley HvHAK1 potassium transporter lead to improved K+-nutrition and enhanced resistance to salt stress. FEBS Lett 582(28):3922–3928. https://doi.org/10.1016/j.febslet.2008.10.036 Mishra M, Wungrampha S, Kumar G, Singla-Pareek SL, Pareek A (2020) How do rice seedlings of landrace Pokkali survive in saline fields after transplantation? Physiology, biochemistry, and photosynthesis. Photosynth Res 150(1-3):117–135. https://doi.org/10.1007/s11120-020-00771-6 Monson RK, Jaeger CH (1991) Photosynthetic characteristics of C3-C4 intermediate Flaveria floridana (Asteraceae) in natural habitats: evidence of advantages to C3-C4 photosynthesis at high leaf temperatures. Am J Bot 78(6):795–800. https://doi.org/10.2307/2445070 Munns R, Day DA, Fricke W, Watt M, Arsova B, Barkla BJ, Bose J, Byrt CS, Chen Z-H, Foster KJ, Gilliham M, Henderson SW, Jenkins CLD, Kronzucker HJ, Miklavcic SJ, Plett D, Roy SJ, Shabala S, Shelden MC, Soole KL, Taylor NL, Tester M, Wege S, Wegner LH, Tyerman SD (2020a) Energy costs of salt tolerance in crop plants. New Phytol 225(3):1072–1090. https://doi.org/10.1111/nph.15864 Munns R, James RA, Läuchli A (2006) Approaches to increasing the salt tolerance of wheat and other cereals. J Exp Bot 57(5):1025–1043. https://doi.org/10.1093/jxb/erj100 Munns R, Passioura JB, Colmer TD, Byrt CS (2020b) Osmotic adjustment and energy limitations to plant growth in saline soil. New Phytol 225(3):1091–1096. https://doi.org/10.1111/nph.15862 Nakamura I, Murayama S, Tobita S, Bong BB, Yanagihara S, Ishimine Y, Kawamitsu Y (2002) Effect of NaCl on the photosynthesis, water relations and free proline accumulation in the wild Oryza species. Plant Prod Sci 5(4):305–310. https://doi.org/10.1626/pps.5.305 Nemati I, Moradi F, Gholizadeh S, Esmaeili M, Bihamta M (2011) The effect of salinity stress on ions and soluble sugars distribution in leaves, leaf sheaths and roots of rice (Oryza sativa L.) seedlings. Plant Soil Environ 57(1):26–33. https://doi.org/10.17221/71/2010-PSE Nieves-Cordones M, Mohamed S, Tanoi K, Kobayashi NI, Takagi K, Vernet A, Guiderdoni E, Périn C, Sentenac H, Véry AA (2017) Production of low-Cs+ rice plants by inactivation of the K+ transporter OsHAK1 with the CRISPR-Cas system. Plant J 92(1):43–56. https://doi.org/10.1111/tpj.13632 Nishizawa Y, Nakamura I, Hossain M, Akamine H, Zheng S (2015) Dry matter production and photosynthetic ability of Oryza officinalis wall ex Watt under salinity stress condition. Jpn J Crop Sci 84(1):49–55. https://doi.org/10.1626/jcs.84.49 Oda Y, Kobayashi NI, Tanoi K, Ma JF, Itou Y, Katsuhara M, Itou T, Horie T (2018) T-DNA tagging-based gain-of-function of OsHKT1;4 reinforces Na exclusion from leaves and stems but triggers Na toxicity in roots of rice under salt stress. Int J Mol Sci 19(1). https://doi.org/10.3390/ijms19010235 Palmgren MG, Edenbrandt AK, Vedel SE, Andersen MM, Landes X, Østerberg JT, Falhof J, Olsen LI, Christensen SB, Sandøe P (2015) Are we ready for back-to-nature crop breeding? Trends Plant Sci 20(3):155–164. https://doi.org/10.1016/j.tplants.2014.11.003 Pan T, Liu MM, Kreslavski VD, Zharmukhamedov SK, Nie CR, Yu M, Kuznetsov VV, Allakhverdiev SI, Shabala S (2021) Nonstomatal limitation of photosynthesis by soil salinity. Crit Rev Environ Sci Technol 51(8):791–825 Pottosin I, Shabala S (2016) Transport across chloroplast membranes: optimizing photosynthesis for adverse environmental conditions. Mol Plant 9(3):356–370 Prusty MR, Kim S-R, Vinarao R, Entila F, Egdane J, Diaz MGQ, Jena KK (2018) Newly identified wild rice accessions conferring high salt tolerance might use a tissue tolerance mechanism in leaf. Front. Plant Sci 9(417). https://doi.org/10.3389/fpls.2018.00417 Queirós F, Fontes N, Silva P, Almeida D, Maeshima M, Gerós H, Fidalgo F (2009) Activity of tonoplast proton pumps and Na+/H+ exchange in potato cell cultures is modulated by salt. J Exp Bot 60(4):1363–1374. https://doi.org/10.1093/jxb/erp011 Radanielson AM, Angeles O, Li T, Ismail AM, Gaydon DS (2018) Describing the physiological responses of different rice genotypes to salt stress using sigmoid and piecewise linear functions. Field Crop Res 220:46–56. https://doi.org/10.1016/j.fcr.2017.05.001 Rajakani R, Sellamuthu G, Ishikawa T, Ahmed HA, Bharathan S, Kumari K, Shabala L, Zhou M, Chen ZH, Shabala S, Venkataraman G (2021) Reduced apoplastic barriers in tissues of shoot-proximal rhizomes of Oryza coarctata are associated with Na+ sequestration. J Exp Bot (in press). https://doi.org/10.1093/jxb/erab440 Rajakani R, Sellamuthu G, Saravanakumar V, Kannappan S, Shabala L, Meinke H, Chen Z, Zhou M, Parida A, Shabala S (2019) Microhair on the adaxial leaf surface of salt secreting halophytic Oryza coarctata Roxb. Show distinct morphotypes: isolation for molecular and functional analysis. Plant Sci 285:248–257. https://doi.org/10.1016/j.plantsci.2019.05.004 Rodríguez-Rosales MP, Jiang X, Gálvez FJ, Aranda MN, Cubero B, Venema K (2008) Overexpression of the tomato K+/H+ antiporter LeNHX2 confers salt tolerance by improving potassium compartmentalization. New Phytol 179(2):366–377. https://doi.org/10.1111/j.1469-8137.2008.02461.x Sage RF (2004) The evolution of C4 photosynthesis. New Phytol 161(2):341–370. https://doi.org/10.1111/j.1469-8137.2004.00974.x Sage RF, Khoshravesh R, Sage TL (2014) From proto-Kranz to C4 Kranz: building the bridge to C4 photosynthesis. J Exp Bot 65(13):3341–3356. https://doi.org/10.1093/jxb/eru180 Schlüter U, Bräutigam A, Gowik U, Melzer M, Christin P-A, Kurz S, Mettler-Altmann T, Weber AP (2017) Photosynthesis in C3–C4 intermediate Moricandia species. J Exp Bot 68(2):191–206. https://doi.org/10.1093/jxb/erw391 Sengupta S, Majumder AL (2010) Porteresia coarctata (Roxb.) Tateoka, a wild rice: a potential model for studying salt-stress biology in rice. Plant Cell Environ 33(4):526–542. https://doi.org/10.1111/j.1365-3040.2009.02054.x Shabala S, Cuin TA (2008) Potassium transport and plant salt tolerance. Physiol Plant 133(4):651–669. https://doi.org/10.1111/j.1399-3054.2007.01008.x Shabala S, Cuin TA, Shabala L, Newman I (2012) Quantifying kinetics of net ion fluxes from plant tissues by non-invasive microelectrode measuring MIFE technique. Plant Salt Tolerance:119–134. https://doi.org/10.1007/978-1-61779-986-0_7 Springer Shabala S, Newman IA, Morris J (1997) Oscillations in H+ and Ca2+ ion fluxes around the elongation region of corn roots and effects of external pH. Plant Physiol 113(1):111–118. https://doi.org/10.1104/pp.113.1.111 Shen Y, Shen L, Shen Z, Jing W, Ge H, Zhao J, Zhang W (2015) The potassium transporter OsHAK21 functions in the maintenance of ion homeostasis and tolerance to salt stress in rice. Plant Cell Environ 38(12):2766–2779. https://doi.org/10.1111/pce.12586 Shenton M, Kobayashi M, Terashima S, Ohyanagi H, Copetti D, Hernández-Hernández T, Zhang J, Ohmido N, Fujita M, Toyoda A (2020) Evolution and diversity of the wild rice Oryza officinalis complex, across continents, genome types, and ploidy levels. Genome Biol Evol 12(4):413–428. https://doi.org/10.1093/gbe/evaa037 Solis CA, Yong MT, Vinarao R, Jena K, Holford P, Shabala L, Zhou M, Shabala S, Chen Z-H (2020) Back to the wild: on a quest for donors toward salinity tolerant rice. Front Plant Sci 11:323. https://doi.org/10.3389/fpls.2020.00323 Sweeney M, McCouch S (2007) The complex history of the domestication of rice. Ann Bot 100(5):951–957. https://doi.org/10.1093/aob/mcm128 Tsujii M, Kera K, Hamamoto S, Kuromori T, Shikanai T, Uozumi N (2019) Evidence for potassium transport activity of Arabidopsis KEA1-KEA6. Sci Rep 9(1):10040. https://doi.org/10.1038/s41598-019-46463-7 Ueno O, Bang SW, Wada Y, Kobayashi N, Kaneko R, Kaneko Y, Matsuzawa Y (2007) Inheritance of C3–C4 intermediate photosynthesis in reciprocal hybrids between Moricandia arvensis (C3–C4) and Brassica oleracea (C3) that differ in their genome constitution. Plant Prod Sci 10(1):68–79. https://doi.org/10.1626/pps.10.68 Vogan PJ, Sage RF (2012) Effects of low atmospheric CO2 and elevated temperature during growth on the gas exchange responses of C3, C3–C4 intermediate, and C4 species from three evolutionary lineages of C4 photosynthesis. Oecologia 169(2):341–352. https://doi.org/10.1007/s00442-011-2201-z von Caemmerer S, Quick WP, Furbank RT (2012) The development of C4 rice: current progress and future challenges. Science 336(6089):1671–1672. https://doi.org/10.1126/science.1220177 Wang F, Chen Z-H, Liu X, Colmer TD, Shabala L, Salih A, Zhou M, Shabala S (2016a) Revealing the roles of GORK channels and NADPH oxidase in acclimation to hypoxia in Arabidopsis. J Exp Bot 68(12):3191–3204. https://doi.org/10.1093/jxb/erw378 Wang F, Chen Z-H, Liu X, Colmer TD, Zhou M, Shabala S (2016b) Tissue-specific root ion profiling reveals essential roles of the CAX and ACA calcium transport systems in response to hypoxia in Arabidopsis. J Exp Bot 67(12):3747–3762. https://doi.org/10.1093/jxb/erw034 Wang F, Chen Z-H, Shabala S (2017a) Hypoxia sensing in plants: on a quest for ion channels as putative oxygen sensors. Plant Cell Physiol 58(7):1126–1142. https://doi.org/10.1093/pcp/pcx079 Wang P, Khoshravesh R, Karki S, Tapia R, Balahadia CP, Bandyopadhyay A, Quick WP, Furbank R, Sage TL, Langdale JA (2017b) Re-creation of a key step in the evolutionary switch from C3 to C4 leaf anatomy. Curr Biol 27(21):3278–3287. e3276. https://doi.org/10.1016/j.cub.2017.09.040 Wang P, Vlad D, Langdale JA (2016c) Finding the genes to build C4 rice. Curr Opin Plant Biol 31:44–50. https://doi.org/10.1016/j.pbi.2016.03.012 Wang S, Cao M, Ma X, Chen W, Zhao J, Sun C, Tan L, Liu F (2017c) Integrated RNA sequencing and QTL mapping to identify candidate genes from Oryza rufipogon associated with salt tolerance at the seedling stage. Front Plant Sci 8:1427. https://doi.org/10.3389/fpls.2017.01427 Waziri A, Kumar P, Purty R (2016) Saltol QTL and their role in salinity tolerance in rice. Austin J Biotechnol Bioeng 3(3):1067 Wu H, Zhang X, Giraldo JP, Shabala S (2018) It is not all about sodium: revealing tissue specificity and signalling roles of potassium in plant responses to salt stress. Plant Soil 431(1):1–17. https://doi.org/10.1007/s11104-018-3770-y Yang Z, Wang C, Xue Y, Liu X, Chen S, Song C, Yang Y, Guo Y (2019) Calcium-activated 14-3-3 proteins as a molecular switch in salt stress tolerance. Nat Commun 10(1):1–12. https://doi.org/10.1038/s41467-019-09181-2 Yeo A, Caporn S, Flowers T (1985) The effect of salinity upon photosynthesis in rice (Oryza sativa L.): gas exchange by individual leaves in relation to their salt content. J Exp Bot 36(8):1240–1248. https://doi.org/10.1093/jxb/36.8.1240 Yichie Y, Brien C, Berger B, Roberts TH, Atwell BJ (2018) Salinity tolerance in Australian wild Oryza species varies widely and matches that observed in O. sativa. Rice 11(1):66. https://doi.org/10.1186/s12284-018-0257-7 Yong M-T, Solis CA, Rabbi B, Huda S, Liu R, Zhou M, Shabala L, Venkataraman G, Shabala S, Chen Z-H (2020) Leaf mesophyll K+ and cl− fluxes and reactive oxygen species production predict rice salt tolerance at reproductive stage in greenhouse and field conditions. Plant Growth Regul 92(1):53–64. https://doi.org/10.1007/s10725-020-00619-y Yorimitsu Y, Kadosono A, Hatakeyama Y, Yabiku T, Ueno O (2019) Transition from C3 to proto-Kranz to C3–C4 intermediate type in the genus Chenopodium (Chenopodiaceae). J Plant Res 132(6):839–855. https://doi.org/10.1007/s10265-019-01135-5 Yoshida S, Forno DA, Cock JH (1971) Laboratory manual for physiological studies of rice. Laboratory Manual for Physiological Studies of Rice, Manila Zepeda-Jazo I, Shabala S, Chen Z, Pottosin II (2008) Na+-K+ transport in roots under salt stress. Plant Signal Behav 3(6):401–403. https://doi.org/10.4161/psb.3.6.5429 Zhang JS, Xie C, Li ZY, Chen SY (1999) Expression of the plasma membrane H+-ATPase gene in response to salt stress in a rice salt-tolerant mutant and its original variety. Theor Appl Genet 99(6):1006–1011. https://doi.org/10.1007/s001220051408 Zong Y, Chen Z, Innes JB, Chen C, Wang Z, Wang H (2007) Fire and flood management of coastal swamp enabled first rice paddy cultivation in East China. Nature 449(7161):459–462. https://doi.org/10.1038/nature06135