SUBJECT INDEX

Acacia, 9–10, 14 Bacillus, 102 Acid stress, 270–273 Bacteroids, 173–177, 226 Aculeiferum, 10 developmental fate of, 175–176 Acyl homoserine lactones (AHL), differentiation, 174–175 263–266 endocytosis, 173–174 Aeschynomene, 13, 331, 338 gene expression in, 266–267 Agrobacterium, 8, 129–130, 132, 139, physiology, 241–276 165, 176, 248, 256, 260–262, signals in, 176–177 270–272 Bean, see Phaseolus Alanine synthesis/metabolism, “β-rhizobia”, 11, 24 248, 296 Biserrula, 37, 382–383, 385 Albizia, 2 Blastobacter, 24–25 Alfalfa, see Medicago Bobgunnia, 11 Allorhizobium, 25 Bradyoxetin, 135–136, 266 Alnus, 2 Bradyrhizobium 25–26, 31–32, 37, Amide export, 303 39, 41, 60, 122, 127–130, 132, γ-aminobutyric acid, see GABA 135–136, 139, 242–251, 254–260, Ammonia assimilation/transport, 262, 266, 269–270, 273, 275, 248, 250 339, 380 Andira, 13 Brucella, 176, 256, 272 Antioxidants in nodules, 345–351 Burkholderia, 11, 24, 26, 379 Arabidopsis, 129, 163–164, 170, 203, 213–217, 307–308, 310, 312, , 9 324, 345, 349 Cajanus, 14, 381 Arachis, 13, 176, 212–213, 217, 364 Calcium gradients, 156–159, 162, Ascorbate peroxidase, 347–348 194–197 Ascorbic acid, 346, 350–351 Calopogonium, 123 Aspalathus, 14 Calystegia, 253 Asparagine synthetase, 309–310 Campsiandra, 9 Aspartate aminotransferase, 308–309 Carbonic anhydrase, 300–301 Aspergillus, 102 CASTOR/CASTOR, 159, 196, Astragalus, 15, 379 202, 229 Ateleia, 11 Casuarina, 2 Atropa, 253 Catalase, 273, 348–349 AUX/AUX, 164–165 Cdk/CDK, 160–161, 172 Auxin, 163–165 Ceanothus, 2 Azorhizobium, 14, 25, 118, 132, 247 Cell cycle, 160–161 Azospirillum, 41, 102, 126, 263 Chaetocalyx, 13 Azotobacter, 322 Chamaecrista, 9, 16, 332

395 396 SUBJECT INDEX

Chamaecytisus, 13 Evolution Chemotaxis and motility, 259–263 of apyrases, 3–6 Chlamydomonas, 203 of hemoglobins, 3–6 Cicer, 365, 367–368, 381 of legumes, 1–21 Cichorium, 371 of mycorrhizas, 3–7 Clitoria, 367, 369 of signals, 3–6 Clover, see Trifolium of symbiosis, 1–21 Colonization of roots, see Root Extracellular polysaccharides (EPS), colonization 134, 142, 162, 265–266, 343 Commercial inoculants, 92–101 Competitiveness, 38–39 Faidherbia, 10 Convolvulus, 253 Flagella, 259–263 Coriaria, 2 Flavonoids, 117–121, 140–143, Cortical-cell activation, 160–169 163–165 Cotton, 39, 384 perception by NodD, 120–121 Cupriavidus, 11, 26 Flemingia, 129 Cyathostegia, 11 Functional genomics, see Genomics cyc/Cyc, 160 Fusarium, 40–41 Cyclolobium, 12, 14 Cyclopia, 14 GABA (γ-aminobutyric acid), 246, 302 Cytokinins, 165 Genes in symbiosis, see Rhizobia or plant symbiotic genes Dahlstedtia, 14 Genome Dalea, 31, 36 conservation, 215–219 Datisca, 2 sequencing, 193, 214–215 Desmanthus, 31 Genomics, 193–194, 211–233 Devosia, 24, 26 Gleditsia, 17 Dicarboxylate metabolism and gln/Gln, 225 transport, 244–247, 251 Gluconeogenesis (rhizobia), 243–244 Dimorphandra, 9 Glutamate synthase (GOGAT), Discolobium, 331 306–308 DMI/DMI, 159–160, 173–174, Glutamine synthetase (GS), 225, 196–199, 201–204, 221, 305–306 230–232 Glutathione, 346–351 Dorycnium, 372 Glutathione peroxidase, 349 Glycine, see Soybean Ecology of root-nodule bacteria, Glycogen metabolism, 247–248 23–43 Glycyrrhiza, 369 Ecto-mycorrhizal fungi, 7, 14 GOGAT, see Glutamate synthase Endo-mycorrhizal fungi, 3–6, 14 Grazielodendron, 13 Enod/ENOD, 162, 167–168, 195, 204, GS, see Glutamine synthetase 332–333 Gunnera, 17 Ensifer, 24, 26 Eriosema, 370 H4/H4, 161 Erythrophleum, 9, 16 HAR/HAR, 196, 204, 231, 233 Ethylene (as hormone), 165–167 HCL/HCL, 159, 222, 231, 233 SUBJECT INDEX 397

Heat stress, 274–275 selecting strains for, 88–92 Hedysarum, 371–372, 379 storage and shelf life for 99–101 Heme peroxidases, 349 technologies for, 77–109 Hemoglobins Iron uptake/use, 254–256 evolution of, 3–6 function, 345 Kalanchöe, 140 occurrence, 323–324 Kennedya, 14 Homoglutathione, see Glutathione Hormones (plant), see Plant hormones Lablab, 369 or nodulation Lactococcus, 200 Host plant, ecosystem fragmentation Lathyrus, 34 by, 36 LAX/LAX, 164–165 Host-plant sanctions, 35–36, 66–70, 176 Leghemoglobin, 323–324, 336–337, Host-symbiont cooperation 344–345 cheating symbionts, 70–71 Legumes explanations for, 61–70 acid and infertile soils, for, mixed nodules, in, 70–71 378–380 problems with, 60–61 agricultural uses of, 366–367 HRGP, 162 anti-helminthic uses of, 371–372 Hydrogenases, 257 aquaculture uses of, 373–374 Hydrogen peroxide (H2O2), 169, 273, breeding constraints of, 367–368, 322–323, 342–344 375–378 Hydroxyl radical, see Reactive oxygen evolution of, 8–17 species fishmeal, as, 373–374 Hymenocarpus, 383 future uses for, 363–386 Hymenolobium, 13 genetic analysis of, 228–230 genomics of, 211–219, 228–233, Indigofera, 14 313–315 Infection, 5, 15–16, 156–159, 191–192 health benefits of, 369–371 Infection thread hydrological stability, for, 375 formation, 156–158 maintaining the symbiosis, growth, 162 382–383 Inocarpus, 13 metabolomics of, 226–228 Inoculation new uses for, 368–380 co-inoculation with PGP pharmaceuticals from, 369–371 organisms, 102–103 production systems using, commercial inoculants for, 92–101 380–384 constraints to, 107–109 proteomics of, 223–226, 315 custom-inoculated seed, 101–102 research advances for, 384–386 formulations for, 93–98 transcriptomics of, 219–223 future prospects for, 105–107 usage patterns, 365–366 need for, 78–88 Lens, 34, 365, 367–368 predicting need for, 86–88 Lessertia, 379–380 pre-inoculated seed, 101–102 Leucaena, 123, 126, 128–129, 244, 252 quality control for, 103–107 Lipochitooligosaccharides, see Nod rhizobia numbers in soil, 81–86 factors 398 SUBJECT INDEX

Lipopolysaccharides (LPS), 142–143, gluconeogenesis, 243–244 177, 343 glycogen of, 247–248 Lolium, 366 malic enzyme, 246 Lotononis, 379 malonate of, 246 Lotus, 14, 17, 63, 122–123, 128–129. metals in, 254–258 142, 162, 165–166, 170, 175, nitrogen, of, 248–251 191–194, 196, 200–201, 203–205, organic acid, of, 244–246, 251 211–223, 226–233, 297, 300, O2 regulation of, 244–245 305–306, 309, 313–314, 330, pentose-phosphate pathway, 242 332–333, 335–337, 345, 348, PHB, of, 247 371–372, 375, 385 polyols, of, 242–243 Lupinus, 13, 38, 170, 248, 300, rhizosphere-associated, 251–253 302–303, 308, 321, 328, 332, sugars, of, 242–243 337, 339–340, 344, 365, 367–368, TCA cycle, 245–246 373–374 vitamins, of, 258 LYK/LYK, 196, 201, 231–232 Metabolism (in nodules) lysR/LysR-type transcriptional allantoin formed in, 303–304 regulator, 118, 121–122, 132 asparagine formed by, 309–310 carbon, of, 296–302 Macroptilium, 123, 128, 130, 136, malate production in, 301–302 139, 244, 367 nitrogen, of, 302–310 Maize, see Zea mays oxaloacetate made by, 299–301 Malate dehydrogenase, 301–302 sugars, of, 294–295, 297–299 Malic enzyme, 246 Metabolomics, 226–228 Malonate metabolism, 246 Metal effects Manganese uptake/use, 258 on legumes, 351 Medicago, 4, 15, 34, 42, 64, 122–123, on root-nodule bacteria, 351 125, 134, 159, 161–162, 164–166, Metarhizium, 102 168, 170–171, 174–175, 177, 179, Methylobacterium, 13, 24, 379 191–194, 196–197, 200–201, Microsynteny, 215–219 203–205, 211–224, 228–233, 244, Mimosa, 9, 11 249–250, 297, 300–303, 306–310, , 9–11 313–314, 322, 325, 331, 333–335, Moldenhauwera, 9 340, 342, 344, 346–349, 351–352, Motility, see Chemotaxis 364–365, 369, 375, 378, 381, 385 Mycorrhiza Melanoxylon, 9 dual infection with, 14, 221 Mesorhizobium, 26, 36–37, 122, evolution of AM, 3–6 128–130, 132, 142, 242, 254–259, evolution of ECM, 7 345, 380, 382–383, 385 infection pathway, 198–199 Metabolism (by rhizobia) Myrica, 2 alanine, 248–249 Myxococcus, 140, 262 ammonium of, 248 C and N linkages, 250 N2 fixation, 177–178 carbon, of, 242–248 O2 effects on, 321–324 Entner-Doudoroff pathway in, 242 NARK/NARK, 204, 231 GABA, of, 246 NCR/NCR, 177 SUBJECT INDEX 399

Nematodes, 7, 371–372 aspartate aminotransferase in, Neptunia, 15, 166, 331–332 308–309 NFP/NFP, 196–197, 198–201, autoregulation in, 204–205 231–232 development of, 3–5, 153–156 NFR/NFR, 196, 200–201, 229, 231–232 differentiation in, 169–173 NGR234, 136–140, 244, 247 endoreduplication in, 169–173 Nickel uptake/use, 258 glutamate synthase in, 306–308 Nif genes, 132–134, 225 glutamine synthetase in, 305–306 NIN/NIN, 196, 203–204, 228–229, glutathione in, 346–351 231–233 hemoglobins in, 323–324, 345 Nissolia, 13 internal O2 of, 324–327, 336–337 N2 fixation, 177–178 leghemoglobin in, 323–324, O2 effects on , 321–324 336–337, 344–345 Nitric oxide, see Reactive nitrogen metabolism in, 226–227, 293–315 species mycorrhizas and, 3–7 Nitrogen assimilation, 302–310 N2 fixation in, 177–178 Nod/noe/nol/nop genes, 105, 122–123, nematode galls and, 7 127, 130–140, 154, 200 nitric oxide in nodules, see Nod boxes, 118–120, 122–132, 135, Reactive nitrogen species 137–139, 140–141 nitrogenase in, 336–337 NodD/NodD, 118–122, 130–140 nutrient exchange in, 225–228 Nod factors, 105, 122–127 O2-diffusion barrier, 324–342 receptors, 199–201 O2 diffusion into, 324–342 signaling, 117–140, 156–160, organic acids in, 294–295 194–199 oxidative stress in, 345–351 synthesis genes, 122–125 pathways for C/N use in, 293–315 Nodulation plant hormones, role of, 163–169 autoregulation of, 204–205 plasmid transfer, 264–265 cell-cycle involvement, 160–161 pollen tubes and, 7–8 ethylene (as hormone) in, 165–167 polyamines in, 227 evolution of, 16 polyols in, 227 hydrogen peroxide (H2O2) in, 169 primitive, 15–16 induction of, 160–169, 191–192 protection from O2 in, 324–342 nitric oxide (NO) in, 169 proteins expressed in, 224–226 plant hormones in, 163–169 reactive nitrogen species (RNS) reactive oxygen species (ROS) in, 322–323, 342–345 in, 169 reactive oxygen species (ROS) in, Nodules 169, 322–323, 342–345 adaptation to O2, 328–331 responses to O2, 324–342 allantoin in, 303–304, 311–313 root involvement in, 6–8 amide export from, 302–304 senescence of, 178–179, 350 amino acids in, 294–296 sugars in, 294–295 antioxidant enzyme in 347–349 supply of C to, 293–302 antioxidants in, 345–347, 350–351 supply of N to, 302–313 asparagine synthetase in, 309–310 transporters in, 227–228 types of, 1–5 400 SUBJECT INDEX

ureide biosynthesis in, 310–313 Phyllobacterium, 24 ureide export from, 302–304 Phyllodineae, 10 Nodulin genes, see ENOD Phytochelatins, 351 NORK/NORK, 159, 231–232 Phytophthora, 102 NSP/NSP, 160, 196–197, 202–203, PIN/PIN, 164–165 205, 221, 231–232 Pisum, 2, 15, 34, 37, 64–65, 125, 142, ntr/Ntr, 225 174, 196, 200–201, 203, 212, 215, 230–233, 242–243, 246, Ochrobactrum, 24 248–249, 296–297, 299–303, O2 diffusion/protection, 324–342 305, 310, 322, 324–325, 328, O2-diffusion barrier in nodules 331–334, 336, 342–344, 346, development of, 336–338 352, 364–365 evidence against, 340–341 Pithecellobium, 11 evidence for, 324–327 Pithium, 40 infected zone, in, 341–342 Plant hormones, 163–169 regulation of, 338–341 Poecilanthe, 12, 14 structure of, 327–336 Pollen tubes, 7–8, 162 Onobrychus, 374, 379 POLLUX/POLLUX, 159, 196, Ormosia, 12 202, 229 Osmotic stress, 268–270 Polyhydroxybutyrate, 64–65, 247 Oxidative stress, 273, 345–351 Primitive nodules, 15–16 Protein-secretion systems Pachyrhizus, 123, 128–129 TFSS type (IV), 129–131, 140, 142 Panicum, 308 TTSS type (III), 128–131, 140, 142 Papilionoideae, 11–15 Proteomics, 223–226 Parasponia, 3, 331–332 Pseudomonas, 4, 40–41, 102, 176 Pea, see Pisum Pterocarpus, 13 Peanut, see Arachis Pueraria, 369 Penicillium, 102 Pentaclethra, 10 Quorum sensing, 34–35, 136, 263–266 Peribacteroid, see Symbiosome Peroxides, see Reactive oxygen species Ralstonia, 11, 24, 26, 121, 139 Peroxiredoxins, 349 Reactive nitrogen species (RNS), Peroxynitrite in nodules, see Reactive 322–323, 342–345 nitrogen species Reactive oxygen species (ROS), 169, Phaseolus, 28–32, 34, 41, 63, 123, 322–323, 342–345 212–213, 215, 271, 297, Rhizobia 299–300, 302–303, 305, 309, biocontrol agents, as, 39–40 311–315, 325, 333, 343–344, chemotaxis by, 259–263 346, 364–365, 381, 385PHB, see co-inoculation with PGP Polyhydroxybutyrate organisms, 102–103 pH effects on rhizobia, see Rhizobia competitiveness of, 38–39 PHB, see Polyhydroxybutyrate diversity in soil, 28–33, 383–384 Phosphate uptake, 274 ecology of, 23–43 Phosphoenolpyruvate carboxylase edaphic factors on, 41–43 (PEPC), 299–300 effect of host diversity, 37–38 SUBJECT INDEX 401

endophytes, as, 39–41 Shepherdia, 2 environmental effects on, 259–266 Sinorhizobium, 27, 31, 34, 40–41, 63, EPS by, 265 158, 162, 174–175, 177, 221–222, host influence on, 33–35 224, 226, 242–265, 267, 269–274, host sanctions on, 35–36, 66–70 343, 347–349, 385 metabolism of, 242–251 Sophora, 11–12 motility of, 259–263 Sorghum, 39 persistence of, 38–39 soybean 31–33, 63, 128–130, 136, pH effects on, 41–42, 270–273 204, 212–217, 219–223, 231–233, physiology of, 241–276 246, 248, 250, 297–298, 300–303, plasmid transfer, 264–265 308–310, 312–315, 321, 327–328, quorum sensing by, 263–266 331, 333–334, 336–341, 343–344, stress responses of, 267–276 346, 349, 364, 369–370, 373–374, symbiotic genes in, 117–142, 381, 384 158–160 Starvation stress, 274–275 nod-box regulation of, 130–140 Streptomyces, 41 temperature effects on, 41–42 Stress responses, 267–276 Rhizobium 26–32, 34, 36, 39–42, 63, Stringent response, 274–275 118, 120, 122–123, 125–126, Stylosanthes, 366 128–134, 136–143, 157, 165, Styphnolobium, 11 175, 200, 242–265, 269–274, Sucrose synthase, 297–299 343, 347, 385 Sugar metabolism, 242–243 Rhizopines, 63–64, 176, 252 Superoxide, see reactive oxygen Rhizosphere and metabolism, species 251–253 Superoxide dismutase (SOD), Rhynchosia, 379 272–273, 342, 347 Rice, 39, 213, 324, 364, 384 SUNN/SUNN, 196, 204, 231, 233 Root colonization, 38–39 Swartzia, 11 Root-hair SYM/SYM, 159, 196, 200–201, calcium gradients, 156–159, 162 203–204, 228–233 deformation, 156–159, Symbiosis 194–195, 198 diversity of, 1–21 Root involvement, 6–8 evolution of, 1–21 Rosid I clade, 1–3 mycorrhizas and, 3–7 Symbiosome membrane proteins, Salinity, effect on rhizobial 223–225 populations, 41 Symbiotic genes, see Rhizobia or plant Salmonella, 176, 249, 255, 259 symbiotic genes Sanctions, see Host-plant sanctions SyrM/SyrM, 132–135, 137–138, Sclerolobium, 9 140–141 Senegalia, 10 Sericia, 371 Tachigali, 9, 16 Sesbania, 14–15, 126, 165–167, 173, of host , 1–21 204, 231–232, 325, 331, 333, Taxonomy of root-nodule bacteria, 336, 338, 342, 352 24–27 402 SUBJECT INDEX

populations, 41–42 Vachellia, 10 Tephrosia, 128, 139 VAM fungi, see Mycorrhiza TFSS systems, see Protein-secretion Vicia, 34, 37, 123, 174, 212, 297, 322, systems 365, 367–368 Thermopsis, 12 Vigna, 126, 129–130, 136, 139, 244, Transcriptomics, 219–223 302–303, 326, 329, 340, 346, Transport 365, 367 amino acids, 249–250 Vitamins, 258 ammonium, 250 Volvox, 200 dicarboxylic acids, 246–247 Trevoa, 2 Wautersia, 11 Trichoderma, 102 Wheat, 39–40, 364 Trifolium, 15, 64, 242, 246, 302–303, 333, 335, 365, 370, 373–378, Xanthomonas, 129, 139 381, 383 Xylella, 139 Trigonella, 370, 375 TTSS systems, see Protein-secretion Zapoteca, 10 systems Zea mays, 310, 348, 364