Supplemental Information
Molecular Evolution of Grass Stomata
Zhong-Hua Chen1,2,*, Guang Chen1, Fei Dai1, Yizhou Wang3, Adrian Hills3, Yong-Ling Ruan4, Guoping Zhang1, Peter J. Franks5, Eviatar Nevo6 and Michael R. Blatt3
1College of Agriculture and Biotechnology, Zhejiang University, Hangzhou 310058, China
2School of Science and Health, Western Sydney University, Penrith, NSW 2751, Australia
3Laboratory of Plant Physiology and Biophysics, University of Glasgow, Glasgow G12 8QQ, United Kingdom
4School of Environmental and Life Sciences, University of Newcastle, Callaghan, NSW 2308, Australia
5Faculty of Agriculture and Environment, The University of Sydney, Sydney, NSW 2006, Australia
6Institute of Evolution, University of Haifa, Mount Carmel, Haifa 31905, Israel
*Correspondence: (Z.H. Chen)
Table S1. Information ofArabidopsis Guard Cell Transporters and ABA Receptor Complex Genes for Evolutionary Bioinformatics Analysis
Genea / Full nameb / Locusb / Gene (bp)b / Protein (aa)b / Functionb / Refs.cAtAKT1 / Arabidopsis K+ transporter 1 / AT2G26650 / 2852 / 857 / A member of the Shaker family inward rectifying potassium channel predominantly expressed in roots, also expressed in guard cells / [1]
AtAKT2 / Arabidopsis K+ transporter 2 / AT4G22200 / 3169 / 802 / A member of the Shaker family inward rectifying potassium channel responsible for the Ca2+ sensitivity of the K+ channel. / [2]
AtKAT1 / potassium channel in Arabidopsis thaliana 1 / AT5G46240 / 2289 / 677 / A member of the Shaker family inward rectifying potassium channel in guard cells / [3;4; 5]
AtKAT2 / potassium channel in Arabidopsis thaliana 2 / AT4G18290 / 2094 / 697 / A member of the Shaker family inward rectifying potassium channel critical to stomatal opening induced by blue light / [6; 7]
AtKAT3 / potassium channel in Arabidopsis thaliana 3 / AT4G32650 / 2197 / 662 / KAT3 does not form functional inward rectifying potassium channel, but down-regulate AKT1 and KAT1 channel activity by forming heteromers with AKT1 or KAT1. / [8]
AtGORK / outwardly-rectifying K+ channel / AT5G37500 / 2860 / 820 / A Shaker family outward rectifying potassium channel in guard cell for stomatal regulation / [9; 10]
AtSLAC1 / slow anion channel-associated 1 / AT1G12480 / 1881 / 556 / Guard cell S-type anion channelregulatesstomatal closure in response to a variety of signals including CO2, ozone, ABA, darkness, and humidity. / [11; 12; 13; 14]
AtSLAH3 / SLAC1 homologue 3 / AT5G24030 / 2389 / 635 / SLAH3 has similarity to SLAC1 and is involved in ion homeostasis in guard cells.
AtALMT6 / aluminium activated malate transporter 6 / AT2G17470 / 1684 / 538 / A member of the aluminum-activated malate transporter family functions as a malate influx or efflux channel in vacuole for stomatal regulation. / [15]
AtALMT9 / aluminium activated malate transporter 9 / AT3G18440 / 2005 / 598 / A member of the aluminum-activated malate transporter family as a vacuolar malate channel / [16]
AtALMT12 / aluminium activated malate transporter 12 / AT4G17970 / 1757 / 560 / A member of the aluminum-activated malate transporter family represents a guard cell plasma membrane R-type anion channel for stomatal closure. / [17; 18]
AtGLR3.1/2 / glutamate receptor 3.1 / AT2G17260 / 3008 / 951 / A plasma membrane glutamate receptor for calcium-programmed stomatal closure. / [19]
AtGLR3.4 / glutamate receptor 3.4 / AT1G05200 / 3257 / 959 / A putative glutamate receptor GLR3 with dual localization in plastid and plasma membrane. / [20]
AtCNGC5 / cyclic nucleotide gated channel 5 / AT5G57940 / 2659 / 717 / A cyclic GMP-activated Ca2+-permeable cation channel in the plasma membrane of guard cells. / [21]
AtCNGC6 / cyclic nucleotide gated channel 6 / AT2G23980 / 2516 / 747 / A cyclic GMP-activated non-selective cation channel in the plasma membrane of guard cells
AtTPK1 / tandem pore K+ channel 1 / AT5G55630 / 1635 / 363 / A member of the TPK/KCO K+ channel family functions as a voltage-independent and Ca2+-activated K+ channel targeted to the tonoplast of guard cell. / [22; 23]
AtTPK3 / tandem pore K+ channel 3 / AT4G18160 / 1501 / 436 / AtTPK3 (KCO6) is a member of the TPK/KCO K+ channel family targeted to the vacuolar membrane of guard cell. / [24]
AtTPC1 / two-pore channel 1 / AT4G03560 / 2674 / 733 / A vacuolar depolarization-activated Ca2+ channel TPC1 is an essential component of the slow vacuolar channel in guard cell for Ca2+ signalling. / [25]
AtAHA1 / H+-ATPase 1 / AT2G18960 / 3431 / 949 / Plasma membrane proton ATPases for stomatal opening and as driving force for nutrient uptake. / [26;27]
AtAHA2 / H+-ATPase 2 / AT4G30190 / 2946 / 981
AtAHA3 / H+-ATPase 3 / AT5G57350 / 3226 / 949
AtAHA4 / H+-ATPase 4 / AT3G47950 / 3220 / 960
AtAHA5 / H+-ATPase 5 / AT2G24520 / 2939 / 931
AtAHA6 / H+-ATPase 6 / AT2G07560 / 3332 / 949
AtAHA7 / H+-ATPase 7 / AT3G60330 / 3235 / 961
AtAHA8 / H+-ATPase 8 / AT3G42640 / 2995 / 948
AtAHA9 / H+-ATPase 9 / AT1G80660 / 2865 / 954
AtAHA10 / H+-ATPase 10 / AT1G17260 / 2488 / 947
AtAHA11 / H+-ATPase 11 / AT5G62670 / 3271 / 956
AtAVP1 / vacuolarpyrophosphatase 1 / AT1G15690 / 2772 / 770 / AtAVP1 contributes to stomatal regulation bycreatingproton driving force for K+ and anion transport into vacuole. / [28]
AtVHA-C / vacuolar ATP synthase subunit C / AT1G12840 / 1491 / 375 / Encodes subunit C of the vacuolar H+-ATPase to regulate stimulus-specific guard cell calcium oscillations and stomatal closure. / [29]
AtVHA-A2 / vacuolar ATP synthase subunit A2 / AT2G21410 / 2860 / 821 / Vacuolar proton ATPase subunit A isoform 2 is required for efficient nutrient storage in vacuole. / [28]
AtACA4 / autoinhibited Ca2+-ATPase 4 / AT2G41560 / 3355 / 1030 / An autoinhibited Ca2+-ATPase localized to the vacuole / [30,
31]
AtACA11 / autoinhibited Ca2+-ATPase 11 / AT3G57330 / 3277 / 1025 / An autoinhibited Ca2+-ATPase localized to the vacuole
AtACA8 / autoinhibited Ca2+-ATPase 8 / AT5G57110 / 3637 / 1074 / An autoinhibited Ca2+ -ATPase isoform 8 localized to the plasma membrane of guard cells / [32;33]
AtACA10 / autoinhibited Ca2+-ATPase 10 / AT4G29900 / 3672 / 1069 / An autoinhibited Ca2+-ATPase localised to the plasma membrane of guard cells.
AtKUP6 / K+ uptake permease 6 / AT1G70300 / 2859 / 782 / Two plasma membrane potassium transporter proteins function in potassium uptake in guard cells. / [34]
AtKUP8 / K+ uptake permease 8 / AT5G14880 / 2346 / 781
AtHKT1 / high-affinity K+ transporter 1 / AT4G10310 / 1755 / 516 / A sodium transporter expressed in xylem parenchyma cells. / [35]
AtNHX1 / Arabidopsis Na+/H+antiporter 1 / AT5G27150 / 2334 / 538 / A vacuolar sodium/proton antiporter involved in salt tolerance, ion homeostasis, and leaf development. / [36;37]
AtNHX2 / Arabidopsis Na+/H+antiporter 2 / AT3G05030 / 2146 / 546 / A vacuolar K+/H+ exchanger essential for active K+ uptake at the tonoplast and involved in regulating stomatal closure.
AtABCC4 / ATP-binding cassette C4 / AT2G47800 / 4847 / 1516 / A plasma membrane ATP-binding cassette (ABC) transporter for stomatal regulation / [38]
AtABCC5 / ATP-binding cassette C5 / AT1G04120 / 5277 / 1514 / A member of ABC transporter subfamily C functions as a high-affinity inositol hexakisphosphate transporter for guard cell signaling and phytate storage. / [39; 40]
AtABCB14 / ATP-binding cassette B14 / AT1G28010 / 3895 / 1247 / An ABC transporter sub family B for stomatal regulation. / [41]
AtCLC-A / chloride channel A / AT5G40890 / 2947 / 775 / Functions as a NO3-/H+ exchanger that serves to accumulate nitrate nutrient in vacuoles. / [42]
AtCLC-B / chloride channel B / AT3G27170 / 2750 / 780 / A member of anion channel protein subfamily B for vacuolar NO3-/H+ exchange / [43]
AtCLC-C / chloride channel C / AT5G49890 / 2836 / 779 / A member ofanion channel protein subfamily C for stomatalregulation / [44]
AtCAX1 / cation exchanger 1 / AT2G38170 / 1596 / 475 / Cation exchangers for high affinity calcium antiporter in guard cells / [45; 30]
AtCAX3 / cation exchanger 3 / AT3G51860 / 1805 / 459
AtSTP1 / sugar transporter 1 / AT1G11260 / 1905 / 552 / A hexose/H+cotransporter for stomatal regulation / [46]
AtSUC3 / sucrose transporter 3 / AT2G02860 / 2318 / 594 / A sucrose transporter / [47]
AtTIP1;1 / tonoplast intrinsic protein 1;1 / AT2G36830 / 1059 / 251 / A tonoplast intrinsic protein in guard cells functions as water channel and the transport of urea and hydrogen peroxide. / [48;49]
AtPIP1;2 / plasma membrane intrinsic protein 1;2 / AT2G45960 / 1299 / 301 / Members of the plasma membrane intrinsic protein subfamily exhibit water transport activity. / [50]
AtPIP2;1 / plasma membrane intrinsic protein 2;1 / AT3G53420 / 1374 / 287 / [51]
AtABI1 / ABA insensitive 1 / AT4G26080 / 2031 / 434 / Protein phosphatase 2Cs are a negative regulators of ABA induced stomatal closure. / [52]
AtABI2 / ABA insensitive 2 / AT5G57050 / 2081 / 423 / [53]
AtHAB1 / hypersensitive to ABA1 / AT1G72770 / 2551 / 511 / A protein phosphatase 2C regulates the activation of the Snf1-related kinase OST1. / [54]
AtRCAR1 / regulatory components of ABA receptor 1 / AT1G01360 / 1000 / 187 / Member of the 14 PYR (pyrabactin resistance)/PYL(PYR1-like)/RCAR (regulatory components of ABA receptor) family proteins, RCAR11/PYR1 functions as one of the abscisic acid sensors. / [11]
AtRCAR10 / regulatory components of ABA receptor 10 / AT2G38310 / 1106 / 207 / [55; 56; 57]
AtRCAR11 / regulatory components of ABA receptor 11 / AT4G17870 / 841 / 191
AtRCAR12 / regulatory components of ABA receptor 12 / AT1G73000 / 833 / 209
AtRCAR14 / regulatory components of ABA receptor 14 / AT2G26040 / 573 / 190
AtOST1 / open stomata 1 / AT4G33950 / 1353 / 362 / A SNF1-related protein kinase (SnRK2) relays between ABA perception and downstream ABA signalling. / [58]
aThisis not a complete list due rapid advancement in new gene discovery in Arabidopsisguard cellsand space limitation. bNomenclatureand information are based on The Arabidopsis Information Resource (TAIR) and relevant references. cReferencesare only selected representatives from the large bulk of literature as not all publications can be listed in the Table.
Table S2.Information of arabidopsis Transporter and ABA Receptor Complex Gene Families for Evolutionary Bioinformatics Analysis
Gene familya / Members (locus)a / Full family namea / Functiona / Refs.bAKTs/KATs/GORKs / AT2G26650, AT4G22200, AT4G32500, AT2G25600, AT5G46240, AT4G18290, AT4G32650, AT5G37500, AT3G02850 / shaker-like K+ channel family / K+ transport in plant cells and stomatalregulation / [59; 60]
SLACs / AT1G12480, AT1G62280, AT4G27970, AT5G24030, AT1G62262 / slow anion channel-associated family / Regulatestomatalclosiure and anion efflux from plant cells / [61]
ALMTs / AT1G08430, AT1G08440, AT1G18420, AT1G25480, AT4G00910, AT1G68600, AT2G17470, AT2G27240, AT3G11680, AT3G18440, AT4G17585, AT4G17970, AT5G46600, AT5G46610 / aluminium activated malate transporter family / Al3+ stress response and stomatal regulation via anion transport / [61]
GLRs / AT3G04110, AT5G48400, AT5G48410, AT3G07520, AT5G27100, AT2G24720, AT2G24710, AT4G31710, AT5G11210, AT5G11180, AT2G29120, AT2G29110, AT2G29100, AT2G17260, AT4G35290, AT1G42540, AT1G05200, AT2G32390, AT3G51480, AT2G32400 / glutamate receptor family / Encode non-selective cation channels / [62]
CNGCs / AT5G53130, AT5G15410, AT2G46430, AT5G54250, AT5G57940, AT2G23980, AT1G15990, AT1G19780, AT4G30560, AT1G01340, AT2G46440, AT2G46450, AT4G01010, AT2G24610, AT2G28260, AT3G48010, AT4G30360, AT5G14870, AT3G17690, AT3G17700 / cyclic nucleotide gated channel family / Permeable to monovalent and divalent cations and putative Ca2+ channels / [63]
TPKs / AT5G55630, AT5G46370, AT4G18160, AT1G02510, AT4G01840 / tandem pore K+ channel family / Vacuolar K+ homeostasis and stomatal regulation / [59]
TPCs / AT4G03560 / two-pore channel family / Voltage-activated slow vacuolar (SV) channels / [64]
AHAs / AT2G18960, AT4G30190, AT5G57350, AT3G47950, AT2G24520, AT2G07560, AT3G60330, AT3G42640, AT1G80660, AT1G17260, AT5G62670, AT4G11730 / H+-ATPase family / Phloem loading, stomatal regulation, root solute uptake and tip growing systems. / [65]
AVPs / AT1G15690, AT1G16780, AT1G78920 / vacuolar H+-pyrophosphatase family / A vacuolar H+ pump for phloem loading and membrane transport of other ions in plant cells. / [66]
VHAs / AT2G28520, AT2G21410, AT4G39080, AT1G12840, AT4G32530, AT4G38920, AT4G34720, AT2G16510, AT1G19910, AT1G75630, AT2G25610, AT1G78900, AT1G76030, AT4G38510, AT1G20260 , AT3G58730, AT4G11150, AT3G08560, AT1G64200, AT4G02620 , AT3G01390, AT4G23710, AT4G25950, AT3G42050, AT3G28710, AT3G28715, AT5G55290, AT4G26710 / vacuolarH+-ATPase family / Essential for cotransport, stomatal regulation, plant development and tolerance to environmental stresses. / [67]
ACAs / AT1G27770, AT4G37640, AT1G07810, AT2G41560, AT3G22910, AT2G22950, AT5G57110, AT3G21180, AT4G29900, AT3G57330, AT3G63380 / autoinhibited Ca2+-ATPase family / Members for plant development, hormones signalling and stress tolerance. / [68]
KT/HAK/KUPs / AT2G30070, AT2G40540, AT3G02050, AT4G23640, AT4G33530, AT4G13420, AT1G70300, AT5G09400, AT5G14880, AT4G19960, AT1G31120, AT2G35060, AT1G60160 / K+ transporter/ high-affinity K+transporter/K+ uptake transporter family / Potassium uptake for cell expansion growth and stomatal regulation / [69;70]
HKTs / AT4G10310 / Trk/HKT family / Function in Na+and K+transport during salinity stress and maintain a high K+/Na+ homeostasis. / [35; 71]
NHXs / AT5G27150, AT3G05030, AT5G55470, AT3G06370, AT1G54370, AT1G79610, AT2G01980, AT1G14660 / Arabidopsis Na+/H+antiporter family / Play a key role in salt tolerance and K+ transport in the vacuole. / [72]
ABCCs / AT1G30400, AT2G34660, AT3G13080, AT2G47800, AT1G04120, AT3G13090, AT3G13100, AT3G21250, AT3G60160, AT3G59140, AT1G30420, AT1G30410, AT2G07680, AT3G62700, AT3G60970 / ATP-binding cassette C subfamily / Play key roles in the efflux of xenobiotic compounds in eukaryotic cells. / [73]
CLCs / AT5G49890, AT5G33280, AT3G27170, AT5G40890, AT5G26240, AT4G35440, AT1G55620 / chloride channel family / Anion channels with various functions / [71]
CAXs / AT2G38170, AT3G13320, AT3G51860, AT5G01490, AT1G55730, AT1G55720, AT5G17860, AT3G14070, AT5G17850, AT1G08960, AT1G54115 / cation exchanger family / Primarily Ca2+ efflux transporters and function in metal transport and abiotic stress tolerance. / [74]
SUCs / AT1G71880, AT1G22710, AT2G02860, AT1G09960, AT5G06170, AT2G14670, AT1G66570, AT5G43610, AT1G71890 / sucrose transporter family / Long distance and membrane transport of sucrose. / [75]
TIPs / AT2G36830, AT3G26520, AT4G01470, AT3G16240, AT5G47450, AT1G52180, AT1G73190, AT1G17810, AT4G17340, AT2G25810, AT3G47440 / tonoplast intrinsic protein family / Water channels and small solute transport. / [76]
PIPs / AT3G61430, AT2G45960, AT1G01620, AT4G00430, AT4G23400, AT3G53420, AT2G37170, AT2G37180, AT5G60660, AT3G54820, AT2G39010, AT2G16850, AT4G35100 / plasma membrane intrinsic protein family / Water channels and small solute transport. / [76]
PP2Cs / AT1G17550, AT4G08260, AT2G40860, AT1G72770, AT3G06270, AT1G78200, AT2G29380, AT3G12620, AT4G31860, AT1G07430, AT1G17545, AT2G34740, AT3G11410, AT3G05640, AT3G15260, AT5G51760, AT4G32950, AT2G20630, AT5G59220, AT3G63320, AT4G28400, AT5G24940, AT5G06750, AT2G25070, AT4G31750, AT2G20050, AT2G20630, AT5G10740, AT3G27140, AT1G09160, AT5G53140, AT3G63340, AT4G31860, AT1G43900, AT3G51370, AT3G16800, AT1G67820, AT1G16220, AT5G66080, AT1G07160, AT5G01700, AT1G68410, AT2G30020, AT4G03415, AT3G51370, AT2G40180, AT5G01700, AT4G38520, AT1G22280, AT1G03590, AT5G26010, AT3G17250, AT4G11040, AT3G17090, AT2G25620, AT1G79630, AT1G18030, AT1G48040, AT3G63340, AT3G55050, AT1G22280, AT1G79630, AT4G27800, AT3G62260, AT2G05050, AT5G02760, AT2G33700, AT5G36250, AT1G47380, AT1G34750, AT3G02750, AT4G33920, AT3G51470, AT5G57050, AT5G27930, AT4G26080 / phytochrome-associated protein phosphatase type 2C family / Act as regulators of signal transduction pathways and also involves in development. / [77; 78]
PYRs/PYLs/RCARs / AT1G01360, AT4G01026, AT5G53160, AT4G27920, AT5G45860, AT5G45870, AT4G18620, AT5G05440, AT2G40330, AT2G38310, AT4G17870, AT5G46790, AT1G73000, AT2G26040 / ABA receptor family / ABA receptors for seed germination, stomatal regulation and stress response / [79]
SnRKs / AT4G33950, AT5G66880, AT3G50500, AT1G10940, AT1G60940, AT5G08590, AT5G63650, AT1G78290, AT4G40010, AT5G25110, AT2G23030, AT3G01090, AT4G24400, AT3G29160, AT5G10930, AT1G30270, AT3G17510, AT2G26980, AT2G34180, AT2G30360, AT1G01140, AT5G39440, AT1G48260, AT3G23000, AT5G35410, AT2G25090, AT4G18700, AT5G01810, AT5G45820, AT5G58380, AT1G29230, AT4G14580, AT2G38490, AT4G30960, AT5G57630, AT5G07070, AT5G01820, AT5G21326, AT5G45810 / SNF1-related protein kinase family / Positive regulators of ABA signalling and many signalling events in plant cells / [80]
aNomenclatureand information are based on The Arabidopsis Information Resource (TAIR) and relevant references.
bReferencesare only selected representatives from the large bulk of literature as not all publications can be listed in the Table.
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