Annual vs. perennial plant evolution

Annuality (living and reproducing in a single year) and perenniality (living more than two years) represent major life history strategies within plant lineages.[1] These traits can shift from one to another over both macroevolutionary and microevolutionary timescales.[2] While perenniality and annuality are often described as discrete either-or traits, they often occur in a continuous spectrum.[2] The complex history of switches between annual and perennial habit involve both natural and artificial causes, and studies of this fluctuation have importance to sustainable agriculture. (Note that "perennial" here refers to both woody and herbaceous perennial species.)

Perennial Silphium integrifolium species (Asteraceae), which is being bred for edible seeds.

According to some studies, either the trait of annuality or perenniality may be ancestral.[3][4] This contradicts the commonly held belief that annuality is a derived trait from an ancestral perennial life form, as is suggested by a regarded plant population biology text.[5]

Spatiotemporal scale

Above the species level, plant lineages clearly vary in their tendency for annuality or perenniality (e.g., wheat vs. oaks). On a microevolutionary timescale, a single plant species may show different annual or perennial ecotypes (e.g., adapted to dry or tropical range), as in the case of the wild progenitor of rice (Oryza rufipogon).[6][7] Indeed, ability to perennate (live more than one year) may vary within a single population of a species.[2][5]

Underlying mechanisms: Trade-offs

Annuality and perenniality are complex traits involving many underlying, often quantitative, genotypic and phenotypic factors.[5][8] They are often determined by a trade-off between allocation to sexual (flower) structures and asexual (vegetative) structures.[9] Switches between the annual and perennial habit are known to be common among herbaceous angiosperms.[9]

Increased allocation to reproduction early in life generally leads to a decrease in survival later in life (senescence); this occurs in both annual and perennial semelparous plants.[5] Exceptions to this pattern include long-lived clonal (see ramets section below) and long-lived non-clonal perennial species (e.g., bristlecone pine).[5]

Associated traits

Many traits involving mating patterns (e.g., outcrossing or selfing) and life history strategies (e.g., annual or perennial) are inherently linked.

Self-fertilization

Self-fertilization (selfing, or autogamy) is more common in annual compared to perennial herbs.[10] Since annuals typically have only one opportunity for reproduction, selfing provides a reliable source of fertilization.[10] However, switches to selfing in annuals may result in an "evolutionary dead end," in the sense that it is probably unlikely to return to an outcrossing (allogamous) state.[10] Selfing and inbreeding can also result in the accumulation of deleterious alleles, resulting in inbreeding depression.[5]

Semelparity
Semelparous vs. iteroparous reproductive strategies.

All annual plants are considered semelparous (a.k.a., monocarpy or big-bang reproduction[11]), i.e., they reproduce once before death.[12] Even semelparity exerts some plasticity in terms of seed-production timing over the year (see "Anomalies" section). That is, it is uncommon for all offspring to be generated at exactly the same time, which would be considered the extreme end of semelparity.[13] Instead offspring are usually generated in discrete packages (as a sort of micro-iteroparous strategy), and the temporal spacing of these reproductive events varies by organism.[13] This is attributed to phenotypic plasticity.[13]

Biennial plants (living two years and reproducing in the second) are also considered semelparous.[12][14]

Seed bank

Although annuals have no vegetative regrowth from year to year, many retain a dormant population back-up underground in the form of a seed bank.[5] The seed bank serves as an annual's source of age structure in the sense that often not all seeds will germinate each year.[5] Thus, each year's population will consist of individuals of different ages in terms of seed dormancy times. The seed bank also helps to ensure the annual's survival and genetic integrity in variable or disturbed habitats (e.g., a desert), where good growing conditions are not guaranteed every year.[5] Not all annuals, however, retain a seed bank.[5] As far as population density, annuals with seed banks are predicted to be more temporally variable yet more spatially constant over time, while plants with no seed bank would be expected to be patchy (spatially variable).[5]

Cross-fertilization

Certain non-selfing reproductive adaptations, such as dioecy (obligate outcrossing via separate male and female individuals), may have arisen in long lived herbaceous and woody species due to negative side effects of selfing in these species, notably genetic load and inbreeding depression.[10] Among angiosperms, dioecy is known to be substantially more common than pure self-incompatibility.[5] Dioecy is also more typical of trees and shrubs compared to annual species.[5]

Iteroparity

Most perennials are iteroparous (or polycarpic), which means they reproduce multiple times during their lifespan.[5]

Rice rhizomes.

Persistence of ramets

Ramets are vegetative, clonal extensions of a central genet. Common examples are rhizomes (modified stem), tillers, and stolons. A plant is perennial if the birth rate of ramets exceeds their death rate.[5] Several of the oldest known plants are clonal. Some genets have been reported to be many thousands of years old, and a steady rate of branching likely aids in avoiding senescence.[5][15][16] The oldest reported minimum age of a single genet is 43,600 years, for Lomatia tasmanica W.M.Curtis.[17] It is hypothesized that some perennial plants even display negative senescence, in which their fecundity and survival increase with age.[16]

Examples of plants with rhizomatous growth include perennial Sorghum and rice, which likely share similar underlying genes controlling rhizome growth.[18][19][20] In wheat (Thinopyrum), perenniality is associated with production of a secondary set of tillers (stems arising from the crown's apical meristem) following the reproductive phase. This is called post-sexual cycle regrowth (PSCR).[8] Such long-lived genets in a population may provide a buffer against random environmental fluctuations.[5]

Polyploidy

There is a possible connection between polyploidy (having more than two copies of one's chromosomes) and perenniality.[3] One potential explanation is that both polyploids (larger in size) and asexual reproduction (common in perennials) tend to be selected for in inhospitable extremes of a species' distribution.[5] One example could be the intricate polyploidy of native Australian perennial Glycine species.[21][22]

Niche conservatism

Woody species have been found to occupy fewer climatic niches than herbaceous species, which was suggested to be a result of their slower generation time; such differences in adaptation may result in niche conservatism among perennial species, in the sense that their climatic niche has not changed much over evolutionary time.[23][24]

Anomalies

Semelparity and iteroparity

Semelparity in perennials is rare but occurs in several types of plants, likely due to adaptive changes for greater seed allocation in response to seed predation (although other drivers, such as biased pollination, have been proposed).[5]

Century plant (Agave deserti) inflorescence; a semelparous perennial.

List of semelparous perennials:[5]

Mating system

The Polemoniaceae (phlox) family shows considerable flexibility in both life history and mating system, showing combinations of annual / selfing, annual / outcrossing, perennial / selfing, and perennial / outcrossing lineages. These switches indicate a more ecologically determined, rather than a phylogenetically fixed, change in habit.[10]

Environmental drivers

High environmental stochasticity, i.e., random fluctuations in climate or disturbance regime, can be buffered by both the annual and perennial habit.[5] However, the annual habit is more closely associated with a stochastic environment, whether that is naturally or artificially induced.[5][25] This is due to higher seedling compared to adult survival in such stochastic environments; common examples are arid environments such as deserts as well as frequently disturbed habitats (e.g., cropland).[5] Iteroparous perennial species are more likely to persist in habitats where adult survival is favored over seedling survival (e.g., canopied, moist).[5] This adult/juvenile trade-off can be described succinctly in the following equations:

λa = cma

λp = cmp + p

ma > (or <) mp + (p/c)[5]

(Silvertown & Charlesworth, 2001, p. 296)

Where: λa = rate of growth of annual population. λp = rate of growth of perennial population. c = survival to reproductive age (flowering). ma = seeds produced for each annual individual (average). mp = seeds produced for each perennial individual. p = adult survival.[5]

If ma > mp + (p/c), the annual habit has greater fitness. If ma < mp + (p/c), the perennial habit has greater fitness.[5] Thus a great deal of the fitness balance depends on the reproductive allocation to seeds, which is why annuals are known for greater reproductive effort than perennials.[5][26]

Different climate and disturbance patterns may also cause demographic changes in populations.[5][27][28]

Evolution rate

The annual vs. perennial trait has been empirically associated with differing subsequent rates of molecular evolution within multiple plant lineages. The perennial trait is generally associated with a slower rate of evolution than annual species when looking at both non-coding[29][30][31] and coding DNA.[32] Generation time is often implicated as one of the major factors contributing to this disparity, with perennials having longer generation times and likewise an overall slower mutation and adaptation rate.[29] This may result in higher genetic diversity in annual lineages.[33]

Plant taxon groups that have evolved both annual and perennial life forms.

Taxon group Shift Reported Cause Sequence-type Geographic Region Literature
Bellis (daisies) perennial→annual aridity nrDNA (ITS) Western Mediterranean [34]
Castilleja (Indian paintbrush) annual→perennial cpDNA (trnL-F, rps16); nrDNA (ITS, ETS) Western North America [3]
Ehrharta (veldtgrass) perennial→annual aridity cpDNA (trnL-F); nrDNA (ITS1) South African Cape [35]
Houstonia perennial→annual cpDNA (trnL-F intron); nrDNA (ITS) [36]
Medicago (alfalfa) annual→perennial

(possibly

perennial→annual

instead)

 nrDNA (ITS, ETS) [4]
Nemesia perennial→annual change in precipitation cpDNA (trnL); nrDNA (ITS, ETS) South African Cape [37]
Oryza (rice) perennial→annual artificial selection for loss of rhizomes coding nuclear DNA Asia [18]
Polemoniaceae (phlox) annual→perennial;

perennial→annual

 ann.→peren.: ecology

peren.→ann.: ecology (desert climate)

 cpDNA (matK) [10]
Sidalcea (checker mallow) perennial→annual aridity nrDNA (ITS, ETS) Western North America [29][30]

Artificial selection

Artificial selection seems to have favored the annual habit, at least in the case of herbaceous species, likely due to fast generation time and therefore a quick response to domestication and improvement efforts.[38] However, woody perennials also exemplify a major group of crops, especially fruit trees and nuts. High yield herbaceous perennial grain or seed crops, however, are virtually nonexistent, despite potential agronomic benefits.[39][40] Several common herbaceous perennial fruit, herbs, and vegetables exist, however; see perennial plants for a list.

Annual and perennial species are known to respond to selection in different ways. For instance, annual domesticates tend to experience more severe genetic bottlenecks than perennial species, which, at least in those clonally propagated, are more prone to continuation of somatic mutations.[1][41] Cultivated woody perennials are also known for their longer generation time, outcrossing with wild species (introducing new genetic variation), and variety of geographic origin.[1] Some woody perennials (e.g., grapes or fruit trees) also have a secondary source of genetic variation within their rootstock (base to which the above-ground portion, the scion, is grafted).[41]

Thinopyrum intermedium: perennial wheat.

Current agricultural applications

Compared to annual monocultures (which occupy c. 2/3 of the world's agricultural land), perennial crops provide protection against soil erosion, better conserve water and nutrients, and undergo a longer growing season.[42][43] Wild perennial species are often more resistant to pests than annual cultivars, and many perennial crop wild relatives have already been hybridized with annual crops to confer this resistance.[42] Perennial species also typically store more atmospheric carbon than annual crops, which can help to mitigate climate change.[42][43] Unfavorable characteristics of such herbaceous perennials include energetically unfavorable trade-offs and long periods of juvenile non-productivity.[41] Some institutions, such as The Land Institute, have begun to develop perennial grains, such as Kernza (perennial wheat), as potential crops.[42] Some traits underlying perenniality may involve relatively simple networks of traits, which can be conferred through hybrid crosses, as in the case of perennial wheat crossed with annual wheat.[8]

See also

References
  1. Miller, Allison J.; Gross, Briana L. (2011-09-01). "From forest to field: Perennial fruit crop domestication". American Journal of Botany. 98 (9): 1389–1414. doi:10.3732/ajb.1000522. ISSN 0002-9122. PMID 21865506.
  2. Fox, Gordon A. (1990-06-01). "Perennation and the Persistence of Annual Life Histories". The American Naturalist. 135 (6): 829–840. doi:10.1086/285076. ISSN 0003-0147. S2CID 85114329.
  3. Tank, David C.; Olmstead, Richard G. (2008-05-01). "From annuals to perennials: phylogeny of subtribe Castillejinae (Orobanchaceae)". American Journal of Botany. 95 (5): 608–625. doi:10.3732/ajb.2007346. ISSN 0002-9122. PMID 21632387.
  4. Bena, G; Lejeune, B; Prosperi, J M; Olivieri, I (1998-06-22). "Molecular phylogenetic approach for studying life-history evolution: the ambiguous example of the genus Medicago L." Proceedings of the Royal Society B: Biological Sciences. 265 (1401): 1141–1151. doi:10.1098/rspb.1998.0410. ISSN 0962-8452. PMC 1689169. PMID 9684377.
  5. Charlesworth, Jonathan; Silvertown, Deborah (2001). Introduction to plant population biology (4th ed.). Oxford [u.a.]: Blackwell Science. p. 165. ISBN 978-0-632-04991-2.
  6. Barbier, P.; Morishima, H.; Ishihama, A. (1991-05-01). "Phylogenetic relationships of annual and perennial wild rice: probing by direct DNA sequencing". Theoretical and Applied Genetics. 81 (5): 693–702. doi:10.1007/BF00226739. ISSN 0040-5752. PMID 24221388. S2CID 36363524.
  7. Khush, Gurdev S. (1997-01-01). "Origin, dispersal, cultivation and variation of rice". In Sasaki, Takuji; Moore, Graham (eds.). Oryza: From Molecule to Plant. Springer Netherlands. pp. 25–34. doi:10.1007/978-94-011-5794-0_3. ISBN 9789401064460.
  8. Lammer, Doug; Cai, Xiwen; Arterburn, Matthew; Chatelain, Jeron; Murray, Timothy; Jones, Stephen (2004-08-01). "A single chromosome addition from Thinopyrum elongatum confers a polycarpic, perennial habit to annual wheat". Journal of Experimental Botany. 55 (403): 1715–1720. doi:10.1093/jxb/erh209. ISSN 0022-0957. PMID 15234999.
  9. Friedman, Jannice; Rubin, Matthew J. (2015-04-01). "All in good time: Understanding annual and perennial strategies in plants". American Journal of Botany. 102 (4): 497–499. doi:10.3732/ajb.1500062. ISSN 0002-9122. PMID 25878083. S2CID 7394680.
  10. Barrett, Spencer C. H.; Harder, Lawrence D.; Worley, Anne C. (1996-09-30). "The Comparative Biology of Pollination and Mating in Flowering Plants". Philosophical Transactions of the Royal Society of London B: Biological Sciences. 351 (1345): 1271–1280. Bibcode:1996RSPTB.351.1271B. doi:10.1098/rstb.1996.0110. ISSN 0962-8436.
  11. Hautekèete, N.-C.; Piquot, Y.; Van Dijk, H. (2001-09-15). "Investment in survival and reproduction along a semelparity–iteroparity gradient in the Beta species complex". Journal of Evolutionary Biology. 14 (5): 795–804. doi:10.1046/j.1420-9101.2001.00322.x. ISSN 1420-9101. S2CID 83176539.
  12. "Semelparity and Iteroparity | Learn Science at Scitable". www.nature.com. Retrieved 2016-04-12.
  13. Hughes, P; Simons, Andrew M (2014-04-26). "The continuum between semelparity and iteroparity: plastic expression of parity in response to season length manipulation in Lobelia inflata". BMC Evolutionary Biology. 14 (1): 90. doi:10.1186/1471-2148-14-90. PMC 4005853. PMID 24766909.
  14. Stratton, Donald A. "Case Studies in Evolutionary Ecology: Why do some species reproduce only once?" (PDF). Plant Biology at the University of Vermont. University of Vermont. Retrieved April 12, 2016.
  15. Inghe, Ola; Tamm, Carl Olof (1985-01-01). "Survival and Flowering of Perennial Herbs. IV. The Behaviour of Hepatica Nobilis and Sanicula Europaea on Permanent Plots during 1943-1981". Oikos. 45 (3): 400–420. doi:10.2307/3565576. JSTOR 3565576.
  16. Munné-Bosch, Sergi (October 2014). "Perennial Roots to Immortality". Plant Physiology. 166 (2): 720–725. doi:10.1104/pp.114.236000. PMC 4213100. PMID 24563283.
  17. Lynch, A. J. J.; Barnes, R. W.; Vaillancourt, R. E.; Cambecèdes, J. (1998). "Genetic Evidence that Lomatia tasmanica (Proteaceae) is an Ancient Clone" (PDF). Australian Journal of Botany. 46 (1): 25–33. doi:10.1071/bt96120. ISSN 1444-9862.
  18. Hu, F. Y.; Tao, D. Y.; Sacks, E.; Fu, B. Y.; Xu, P.; Li, J.; Yang, Y.; McNally, K.; Khush, G. S.; Paterson, A. H.; Li, Z.- K. (17 March 2003). "Convergent evolution of perenniality in rice and sorghum". Proceedings of the National Academy of Sciences. 100 (7): 4050–4054. Bibcode:2003PNAS..100.4050H. doi:10.1073/pnas.0630531100. PMC 153046. PMID 12642667.
  19. Kong, Wenqian; Kim, Changsoo; Goff, Valorie H.; Zhang, Dong; Paterson, Andrew H. (2015-05-01). "Genetic analysis of rhizomatousness and its relationship with vegetative branching of recombinant inbred lines of Sorghum bicolor × S. propinquum". American Journal of Botany. 102 (5): 718–724. doi:10.3732/ajb.1500035. ISSN 0002-9122. PMID 26022486.
  20. Paterson, A. H.; Schertz, K. F.; Lin, Y. R.; Liu, S. C.; Chang, Y. L. (1995-06-20). "The weediness of wild plants: molecular analysis of genes influencing dispersal and persistence of johnsongrass, Sorghum halepense (L.) Pers". Proceedings of the National Academy of Sciences of the United States of America. 92 (13): 6127–6131. Bibcode:1995PNAS...92.6127P. doi:10.1073/pnas.92.13.6127. ISSN 0027-8424. PMC 41655. PMID 11607551.
  21. Doyle, J. J.; Doyle, J. L.; Brown, A. H. D. (1999-09-14). "Origins, colonization, and lineage recombination in a widespread perennial soybean polyploid complex". Proceedings of the National Academy of Sciences. 96 (19): 10741–10745. Bibcode:1999PNAS...9610741D. doi:10.1073/pnas.96.19.10741. ISSN 0027-8424. PMC 17953. PMID 10485896.
  22. Doyle, Jeff J.; Doyle, Jane L.; Rauscher, Jason T.; Brown, A. H. D. (14 November 2003). "Diploid and polyploid reticulate evolution throughout the history of the perennial soybeans (Glycine subgenus Glycine)". New Phytologist. 161 (1): 121–132. doi:10.1046/j.1469-8137.2003.00949.x.
  23. Smith, Stephen A.; Beaulieu, Jeremy M. (2009-12-22). "Life history influences rates of climatic niche evolution in flowering plants". Proceedings of the Royal Society of London B: Biological Sciences. 276 (1677): 4345–4352. doi:10.1098/rspb.2009.1176. ISSN 0962-8452. PMC 2817099. PMID 19776076.
  24. Diniz-Filho, José Alexandre Felizola; Terribile, Levi Carina; da Cruz, Mary Joice Ribeiro; Vieira, Ludgero Cardoso G. (2010-11-01). "Hidden patterns of phylogenetic non-stationarity overwhelm comparative analyses of niche conservatism and divergence". Global Ecology and Biogeography. 19 (6): 916–926. doi:10.1111/j.1466-8238.2010.00562.x. ISSN 1466-8238.
  25. Harper, John L. (1977). Population biology of plants. London, England: Academic Press. ISBN 978-1932846249.
  26. Lamont C. Cole. "The Population Consequences of Life History Phenomena." The Quarterly Review of Biology 29, no. 2 (June 1954): 103-137
  27. van Groenendael, J. M.; Slim, P. (1988-01-01). "The Contrasting Dynamics of Two Populations of Plantago Lanceolata Classified by Age and Size". Journal of Ecology. 76 (2): 585–599. doi:10.2307/2260614. JSTOR 2260614.
  28. van Groenendael, J (1985). "Differences in life histories between two ecotypes of Plantago lanceolata L.". In White, J. (ed.). Studies on plant demography. London, England: Academic Press. pp. 51–67.
  29. Andreasen, K; Baldwin, BG (June 2001). "Unequal evolutionary rates between annual and perennial lineages of checker mallows (Sidalcea, Malvaceae): evidence from 18S-26S rDNA internal and external transcribed spacers". Molecular Biology and Evolution. 18 (6): 936–44. doi:10.1093/oxfordjournals.molbev.a003894. PMID 11371581.
  30. Andreasen, Katarina; Baldwin, Bruce G. (2003-03-01). "Reexamination of relationships, habital evolution, and phylogeography of checker mallows (Sidalcea; Malvaceae) based on molecular phylogenetic data". American Journal of Botany. 90 (3): 436–444. doi:10.3732/ajb.90.3.436. ISSN 0002-9122. PMID 21659137.
  31. Laroche, J.; Bousquet, J. (1999-04-01). "Evolution of the mitochondrial rps3 intron in perennial and annual angiosperms and homology to nad5 intron 1". Molecular Biology and Evolution. 16 (4): 441–452. doi:10.1093/oxfordjournals.molbev.a026126. ISSN 0737-4038. PMID 10331271.
  32. Bousquet, J.; Strauss, S. H.; Doerksen, A. H.; Price, R. A. (1992-08-15). "Extensive variation in evolutionary rate of rbcL gene sequences among seed plants". Proceedings of the National Academy of Sciences. 89 (16): 7844–7848. Bibcode:1992PNAS...89.7844B. doi:10.1073/pnas.89.16.7844. ISSN 0027-8424. PMC 49808. PMID 1502205.
  33. Xu, Xin-Wei; Wu, Jin-Wei; Qi, Mei-Xia; Lu, Qi-Xiang; Lee, Peter F.; Lutz, Sue; Ge, Song; Wen, Jun (2015-02-01). "Comparative phylogeography of the wild-rice genus Zizania (Poaceae) in eastern Asia and North America". American Journal of Botany. 102 (2): 239–247. doi:10.3732/ajb.1400323. ISSN 0002-9122. PMID 25667077.
  34. Fiz, Omar; Valcárcel, Virginia; Vargas, Pablo (2002-10-01). "Phylogenetic position of Mediterranean Astereae and character evolution of daisies (Bellis, Asteraceae) inferred from nrDNA ITS sequences". Molecular Phylogenetics and Evolution. 25 (1): 157–171. doi:10.1016/S1055-7903(02)00228-2. PMID 12383758.
  35. Verboom, G. Anthony; Linder, H. Peter; Stock, William D.; Baum, D. (2003-05-01). "Phylogenetics of the grass genus ehrharta: evidence for radiation in the summer-arid zone of the South African cape". Evolution. 57 (5): 1008–1021. doi:10.1554/0014-3820(2003)057[1008:POTGGE]2.0.CO;2. ISSN 0014-3820. PMID 12836819. S2CID 198155475.
  36. Church, Sheri A (2003-05-01). "Molecular phylogenetics of Houstonia (Rubiaceae): descending aneuploidy and breeding system evolution in the radiation of the lineage across North America". Molecular Phylogenetics and Evolution. 27 (2): 223–238. doi:10.1016/S1055-7903(02)00446-3. PMID 12695087.
  37. Datson, P. M.; Murray, B. G.; Steiner, K. E. (4 December 2007). "Climate and the evolution of annual/perennial life-histories in Nemesia (Scrophulariaceae)". Plant Systematics and Evolution. 270 (1–2): 39–57. doi:10.1007/s00606-007-0612-4. S2CID 11649979.
  38. Zeder, Melinda A.; Emshwiller, Eve; Smith, Bruce D.; Bradley, Daniel G. (2006-03-01). "Documenting domestication: the intersection of genetics and archaeology". Trends in Genetics. 22 (3): 139–155. doi:10.1016/j.tig.2006.01.007. ISSN 0168-9525. PMID 16458995.
  39. Van Tassel, David L.; DeHaan, Lee R.; Cox, Thomas S. (2010-09-01). "Missing domesticated plant forms: can artificial selection fill the gap?". Evolutionary Applications. 3 (5–6): 434–452. doi:10.1111/j.1752-4571.2010.00132.x. ISSN 1752-4571. PMC 3352511. PMID 25567937.
  40. Glover, Jerry D.; Reganold, John P. (2010). "Perennial Grains: Food Security for the Future" (PDF). Issues in Science and Technology. 26 (2): 41–47.
  41. Gaut, Brandon S.; Díez, Concepción M.; Morrell, Peter L. (December 2015). "Genomics and the Contrasting Dynamics of Annual and Perennial Domestication". Trends in Genetics. 31 (12): 709–719. doi:10.1016/j.tig.2015.10.002. PMID 26603610.
  42. Cox, Thomas S.; Glover, Jerry D.; Tassel, David L. Van; Cox, Cindy M.; DeHaan, Lee R. (2006-08-01). "Prospects for Developing Perennial Grain Crops". BioScience. 56 (8): 649–659. doi:10.1641/0006-3568(2006)56[649:PFDPGC]2.0.CO;2. ISSN 0006-3568.
  43. Kell, Douglas B. (2011-09-01). "Breeding crop plants with deep roots: their role in sustainable carbon, nutrient and water sequestration". Annals of Botany. 108 (3): 407–418. doi:10.1093/aob/mcr175. ISSN 0305-7364. PMC 3158691. PMID 21813565.
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